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Short- and long-term temporal changes in the assemblage structure of Amazonian dung beetles

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Abstract

Species diversity varies in space and time. Temporal changes in the structure and dynamics of communities can occur at different scales. We investigated the temporal changes of dung beetle assemblages in the Amazonian region along seasons, years, and successional stages. We evaluated if assemblage structure changes between temporal scales and whether such changes affect the functional structure of communities. To achieve these goals, we sampled dung beetles using linear transects of baited pitfall traps during the dry and rainy seasons at two natural reserves in the Amazon region, each representing different time scales: one covering successional variations (80, 30, 5, and 1 years of recovery from logging) and the other one encompassing three consecutive years at two successional stages (20 and 10 years from logging). We used Generalized Linear Models to analyze interannual and successional changes in diversity, described assemblage structure with a NMDS, and examined compositional variation by partitioning beta diversity into its nestedness and turnover components. Abundance and richness decrease from the rainy to the dry season and towards earlier successional stages but do not differ between years. Assemblage diversity changes differently in interannual and successional scales. During succession, dung beetle assemblages change drastically, following a nested structure due to the appearance of species and functional groups in later successional stages. In contrast, functional group composition does not show consistent changes between years, displaying a turnover structure. This pattern supports non-deterministic changes in dung beetle assemblage structure along forest succession.

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References

  • Agoglitta R, Moreno CE, Zunino M, Bonsignori G, Dellacasa M (2012) Cumulative annual dung beetle diversity in Mediterranean seasonal environments. Ecol Res 27:387–395

    Article  Google Scholar 

  • Andrade RB, Barlow J, Louzada J, Vaz-de-Mello FZ, Souza M, Silveira JM, Cochrane MA (2011) Quantifying responses of dung beetles to fire disturbance in tropical forests: the importance of trapping method and seasonality. PLoS ONE 6:e26208

    Article  PubMed  PubMed Central  Google Scholar 

  • Andresen E (2002) Dung beetles in a Central Amazonian rainforest and their ecological role as secondary seed dispersers. Ecol Entomol 27:257–270

    Article  Google Scholar 

  • Andresen E (2005) Effects of season and vegetation type on community organization of dung beetles in a tropical dry forest. Biotropica 37:291–300

    Article  Google Scholar 

  • Audino LD, Louzada J, Comita L (2014) Dung beetles as indicators of tropical forest restoration success: Is it possible to recover species and functional diversity? Biol Conserv 169:248–257

    Article  Google Scholar 

  • Bang HS, Lee JH, Kwon OS, Na YE, Jang YS, Kim WH (2005) Effects of paracoprid dung beetles (Coleoptera: Scarabaeidae) on the growth of pasture herbage and on the underlying soil. Appl Soil Ecol 29:165–171

    Article  Google Scholar 

  • Barlow J, Gardner TA, Araujo IS, Avila-Pires TC, Bonaldo AB, Costa JE, Esposito MC, Ferreira LV, Hawes J, Hernandez MIM, Hoogmoed MS, Leite RN, Lo-Man-Hung NF, Malcolm JR, Marins MB, Mestre LAM, Miranda-Samtos R, Nunes-Gutjahr AL, Overal WL, Parry L, Peters SL, Ribeiro-Junior MA, Da Silva MNF, Motta CS, Peres CA (2007) Quantifying the biodiversity value of tropical primary, secondary and plantation forests. Proc Nat Acad Sci USA 104:18555–18560

    Article  CAS  PubMed  Google Scholar 

  • Barragan F, Moreno CE, Escobar F, Halffter G, Navarrete D (2011) Negative impacts of human land use on dung beetle functional diversity. PLoS ONE 6:e17976

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baselga A (2010) Partitioning the turnover and nestedness components of beta diversity. Global Ecol Biogeogr 19:134–143

    Article  Google Scholar 

  • Baselga A, Orme CDL (2012) betapart: an R package for the study of beta diversity. Met Ecol Evol 3:808–812

    Article  Google Scholar 

  • Beiroz W, Slade EM, Barlow J, Silveira JM, Louzada J, Sayer E (2017) Dung beetle community dynamics in undisturbed tropical forests: implications for ecological evaluations of land-use change. Insect Conserv Diver 10:94–106

    Article  Google Scholar 

  • Beiroz W, Sayer E, Slade EM, Audino L, Braga RF, Louzada J, Barlow J (2018) Spatial and temporal shifts in functional and taxonomic diversity of dung beetles in a human-modified tropical forest landscape. Ecol Indic 95:518–526

    Article  Google Scholar 

  • Bicknell JE, Phelps SP, Davies RG, Mann DJ, Struebig MJ, Davies ZG (2014) Dung beetles as indicators for rapid impact assessments: Evaluating best practice forestry in the neotropics. Ecol Indic 43:154–161

    Article  Google Scholar 

  • Braga RF, Korasaki V, Andresen E, Louzada J (2013) Dung beetle community and functions along a habitat-disturbance gradient in the Amazon: a rapid assessment of ecological functions associated to biodiversity. PLoS ONE 8:e57786

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New York, p 488

    Google Scholar 

  • Cajaiba RL, Perico E, Dalzochio MS, da Silva WB, Bastos R, Cabral JA, Santos M (2017) Does the composition of Scarabaeidae (Coleoptera) communities reflect the extent of land use changes in the Brazilian Amazon? Ecol Indic 74:285–294

    Article  Google Scholar 

  • Cambefort Y, Hanski I (1991) Dung beetle population biology. In: Hanski I, Cambefort Y (eds) Dung beetle ecology. Princeton University, Princeton, New Jersey, USA, pp 37–50

    Google Scholar 

  • Camero E (2010) Los escarabajos del género Eurysternus Dalman, 1824 (Coleoptera: Scarabaeidae) de Colombia. Bol Soc Entomol Arag 46:147–179

    Google Scholar 

  • Clements FE (1916) Plant succession. In: An analysis of the development of vegetation, vol 242. Carnegie Institution of Washington, Washington DC, 512 p

  • Colwell RK (2016) EstimateS: Statistical estimation of species richness and shared species from samples. Version 9.1.0. User’s guide and applications. http://viceroy.eeb.uconn.edu/estimates

  • Connell JH, Slatyer RO (1977) Mechanisms of succession in natural communities and their role in community stability and organization. Am Nat 111:119–144

    Article  Google Scholar 

  • Cook J (2002) A revision of the neotropical genus Cryptocanthon. Coleopt Soc Monogr 1:1–96

    Google Scholar 

  • Cuesta E, Lobo JM (2019) A comparison of dung beetle assemblages (Coleoptera, Scarabaeoidea) collected 34 years apart in an Iberian mountain locality. J Insect Conserv 23:101–110

    Article  Google Scholar 

  • Cupello M, Vaz-de-Mello FZ (2013) Taxonomic revision of the South American dung beetle genus Gromphas Brullé, 1837 (Coleoptera: Scarabaeidae: Sacrabaeinae: Phanaeini: Gromphadina). Zootaxa 3722:439–482

    Article  PubMed  Google Scholar 

  • Da Silva PG, Hernández MIM (2015) Scale-dependence of processes structuring dung beetle metacommunities using functional diversity and community deconstruction approaches. PLoS ONE 10(3):e0123030

    Article  PubMed  PubMed Central  Google Scholar 

  • Da Silva PG, Hernández MIM (2018) Spatial but not temporal dung beetle β-diversity components are scale-dependent in a mainland-island scenario. Austr Ecol 43:915–925

    Article  Google Scholar 

  • Davis AJ, Holloway JD, Huijbregts H, Krikken J, Kirk-Spriggs AH, Sutton SL (2001) Dung beetles as indicators of change in the forests of northern Borneo. J Appl Ecol 38:593–616

    Article  Google Scholar 

  • Denslow JS (1980) Patterns of plant species diversity during succession under different disturbance regimes. Oecologia 46:18–21

    Article  PubMed  Google Scholar 

  • Dijkstra JA, Westerman EL, Harris LG (2011) The effects of climate change on species composition, succession and phenology: a case study. Global Change Biol 17:2360–2369

    Article  Google Scholar 

  • Doube B (1990) A functional classification for analysis of the structure of dung beetle assemblages. Ecol Entomol 15:371–383

    Article  Google Scholar 

  • Edmonds WD (1994) Revision of Phanaeus Macleay, a new world genus of Scarabaeine dung beetles (Coleoptera: Scarabaeidae, Scarabaeinae). Contr Sci NHM Angeles Ctry 443:1–105

    Article  Google Scholar 

  • Edmonds WD, Zídek J (2004) Revision of the Neotropical dung beetle genus Oxysternon (Scarabaeidae: Scarabaeinae: Phanaeini). Folia Heyrovskyana Suppl 11:1–58

    Google Scholar 

  • Edmonds WD, Zídek J (2010) A taxonomic review of the neotropical genus Coprophanaeus Olsoufieff, 1924 (Coleoptera: Scarabaeidae, Scarabaeinae). Insect Mundi 0129:1–111

    Google Scholar 

  • Edwards FA, Finan J, Graham LK, Larsen TH, Wilcove DS, Hsu WW, Chey VK, Hamer KC (2017) The impact of logging roads on dung beetle assemblages in a tropical rainforest reserve. Biol Conserv 205:85–92

    Article  PubMed  PubMed Central  Google Scholar 

  • Encinas-Viso F, Revilla TA, Etienne RS (2012) Phenology drives mutualistic network structure and diversity. Ecol Lett 15:198–208

    Article  PubMed  Google Scholar 

  • Escobar F, Halffter G, Solis A, Halffter V, Navarrete D (2008) Temporal shifts in dung beetle community structure within a protected are of tropical wet forest: a 35-year study and its implications for long-term conservation. J Appl Ecol 45:1584–1592

    Article  Google Scholar 

  • Estrada A, Halffter G, Coates-Estrada R, Merrit DA (1993) Dung beetles attracted to mammalian hervibore (Alouatta palliata) and omnivore (Nasua narica) dung in the tropical rain forest of Los Tuxtlas, Mexico. J Trop Ecol 9:45–54

    Article  Google Scholar 

  • Feer F, Boissier O (2015) Variations in dung beetle assemblages across a gradient of hunting in a tropical forest. Ecol Ind 57:164–170

    Article  Google Scholar 

  • Ferreira SC, Da Silva PG, Paladini A, Di Mare RA (2019) Climatic variables drive temporal patterns of α and β diversities of dung beetles. Bull Entomol Res 109:390–397

    Article  CAS  PubMed  Google Scholar 

  • Forister ML, McCall AC, Sanders NJ, Fordyce JA, Thorne JH, O’Brien J, Waetjen DP, Shapiro AM (2010) Compounded effects of climate change and habitat alteration shift patterns of butterfly diversity. Proc Nat Acad Sci USA 107:2088–2092

    Article  CAS  PubMed  Google Scholar 

  • Franca F, Louzada J, Korasaki V, Griffiths H, Silveira JM, Barlow J (2016) Do space-for-time assessments underestimate the impacts of logging on tropical biodiversity? An Amazonian case study using dung beetles. J Appl Ecol 53:1098–1105

    Article  Google Scholar 

  • Fritz SA, Schnitzler J, Eronen JT, Hof C, Bohning-Gaese K, Graham CH (2013) Diversity in time and space: wanted dead and alive. Trends Ecol Evol 28:509–516

    Article  PubMed  Google Scholar 

  • Gardner TA, Hernández MIM, Barlow J, Peres CA (2008) Understanding the biodiversity consequences of habitat change: the value of secondary and plantation forests for neotropical dung beetles. J Appl Ecol 45:883–893

    Article  Google Scholar 

  • Genier F (1996) A revision of the neotropical genus Ontherus Erichson (Coleoptera: Scarabaeidae, Scarabaeinae). Mem Entomol Soc Canada 170:1–168

    Google Scholar 

  • Gleason HA (1927) Further views on the succession concept. Ecology 8:299–326

    Article  Google Scholar 

  • Grimbacher PS, Stork NE (2009) Seasonality of a diverse beetle assemblage inhabiting lowland tropical rain forest in Australia. Biotropica 41:328–337

    Article  Google Scholar 

  • Grøtan VR, Lande R, Engen S, Sæther BE, DeVries PJ (2014) Seasonal cycles of diversity and similarity in a Central American rainforest butterfly community. Ecography 37:509–516

    Google Scholar 

  • Halffter G, Arellano L (2002) Response of dung beetle diversity to human-induced changes in a tropical landscape. Biotropica 34:144–154

    Article  Google Scholar 

  • Halffter G, Edmonds WD (1982) The nesting behaviour of dung beetles (Scarabaeinae): an ecological and evolutive approach. Instituto de Ecología, MAB-UNESCO, México, DF

    Google Scholar 

  • Halffter G, Matthews EG (1966) The natural history of dung beetles of the subfamily Scarabaeinae. Folia Entomol Mex 12–14:1–312

    Google Scholar 

  • Hanski I (1982) Dynamics of regional distribution: the core and satellite species hypothesis. Oikos 38:210–221

    Article  Google Scholar 

  • Hernández MIM, Vaz-de-Mello FZ (2009) Seasonal and spatial species richness variation of dung beetle (Coleoptera, Scarabaeidae s. str.) in the Atlantic forest of southeastern Brazil. Rev Brasil Entomol 53(4):607–613

    Article  Google Scholar 

  • Hewitt JE, Thrush SF, Ellingsen KE (2016) The role of time and species identities in spatial patterns of species richness and conservation. Conserv Biol 30(5):1080–1088

    Article  PubMed  Google Scholar 

  • Higgins MA, Ruokolainen K, Tuomisto H, Llerena N, Cardenas G, Phillips OL, Vásquez R, Räsänen M (2011) Geological control of floristic composition in Amazonian forests. J Biogeogr 38:2136–2149

    Article  PubMed  PubMed Central  Google Scholar 

  • Hodgson JA, Thomas CD, Oliver TH, Anderson BJ, Brereton TM, Crone EE (2010) Predicting insect phenology across space and time. Global Change Biol 17:1289–1300

    Article  Google Scholar 

  • Horgan FG (2008) Dung beetle assemblages in forests and pastures of El Salvador: a functional comparison. Biodiv Conserv 17:2961–2978

    Article  Google Scholar 

  • Hortal J, De Marco P, Santos AMC, Diniz-Filho AF (2012) Integrating biogeographical processes and local community assembly. J Biogeogr 39:627–628

    Article  Google Scholar 

  • Hosaka T, Niino M, Kon M, Ochi T, Yamada T, Fletcher C, Okuda T (2014) Effects of logging road networks on the ecological functions of dung beetles in Peninsular Malaysia. For Ecol Manage 326:18–24

    Article  Google Scholar 

  • Howden HF, Nealis VG (1975) Effects of clearing in a tropical rain forest on the composition of the coprophagous scarab beetle fauna (Coleoptera). Biotropica 7:77–83

    Article  Google Scholar 

  • INPA (2017) PRODES—Monitoramento da Floresta Amazônica Brasileira por Satélite. Instituto Nacional de Pesquisas Espaciais, São José dos Campos, São Paulo, Brasil. http://www.obt.inpe.br/prodes/dashboard/prodes-rates.html Accessed 30 Jan 2018

  • Kishimoto-Yamada K, Itioka T (2015) How much have we learned about seasonality in tropical insect abundance since Wolda (1988)? Entomol Sci 18:407–419

    Article  Google Scholar 

  • Korasaki V, Vaz-De-Mello FZ, Braga RF, Zanetti R, Louzada J (2013) Conservation value of alternative land-use systems for dung beetles in Amazon: valuing traditional farming practices. Biodiv Conserv 22:1485–1499

    Article  Google Scholar 

  • Labidi I, Erroussi F, Nouira S (2012) Spatial and temporal variation in species composition, diversity, and structure of mediterranean dung beetle assemblages (Coleoptera: Scarabaeidae) across a bioclimatic gradient. Environ Entomol 41:785–801

    Article  Google Scholar 

  • Larsen TH, Forsyth A (2005) Trap spacing and transect design for dung beetle biodiversity studies. Biotropica 37:322–325

    Article  Google Scholar 

  • Lenth RV (2016) Least-squares means: The R package lsmeans. J Stat Softw 69(1):1–33

    Article  Google Scholar 

  • Lobo JM (2001) Decline of roller dung beetle (Scarabaeinae) populations in the Iberian península during the 20th century. Biol Conserv 97:43–50

    Article  Google Scholar 

  • Lobo JM (2008) Database records as a surrogate for sampling effort provide higher species richness estimations. Biodiv Conserv 17:873–881

    Article  Google Scholar 

  • Lopes J, Korasaki V, Catelli L, Marcai VVM, Nunes MPBP (2011) A comparison of dung beetle assemblage structure (Coleoptera: Scarabaeidae: Scarabaeinae) between an Atlantic forest fragment and adjacent abandoned pasture in Paraná, Brazil. Zoologia 28:72–79

    Article  Google Scholar 

  • Losey JE, Vaughan M (2006) The economic value of ecological services provided by insects. Bioscience 56:311–323

    Article  Google Scholar 

  • Matos P, Pinho P, Aragón G, Martínez I, Nunes A, Soares AMVM, Branquinho C (2015) Lichen traits responding to aridity. J Ecol 103:451–458

    Article  Google Scholar 

  • McCune B, Grace JB (2002) Analysis of ecological communities. MjM software design, Gleneden Beach, Oregon

    Google Scholar 

  • McGeoch MA, van Rensburg BJ, Botes A (2002) The verification and application of bioindicators: a case study of dung beetles in a savanna ecosystem. J Appl Ecol 39:661–672

    Article  Google Scholar 

  • Menéndez R (1994) Patrones de distribución y abundancia en especies de escarabajos coprófagos. Stvdia Oecol 10–11:395–400

    Google Scholar 

  • Milotic T, Blatzinger C, Eichberg C, Eycott AE, Heurich M, Müller J, Noriega JA, Menendez R, Stadler J, Ádám R, Bargamnn T, Bilger I, Buse J, Calatayud J, Ciubuc C, Boros G, Jay-Robert P, Kruus M, Merivee E, Miessen G, Must A, Ardali E, Preda E, Rahimi I, Rohwedder D, Rose R, Slade EM, Somay L, Tahmasebi P, Ziani S, Hoffman M (2018) Functionally richer communities improve ecosystem functioning: dung removal and secondary seed dispersal by dung beetles in the Western Palaearctic. J Biogeogr 46:70–82

    Article  Google Scholar 

  • Nichols E, Uriarte M, Bunker DE, Favila ME, Slade EM, Vulinec K, Larsen T, Vaz-de-Mello FZ, Louzada J, Naeem S, Spector SH (2013) Trait-dependent response of dung beetle populations to tropical forest conversion at local and regional scales. Ecology 94:180–189

    Article  PubMed  Google Scholar 

  • Nichols E, Larsen T, Spector S, Davies AL, Escobar F, Favila M, Vulinec K, The Scarabaeinae Research Network (2007) Global dung beetle response to tropical forest modification and fragmentation: a quantitative literature review and meta-analysis. Biol Conserv 137:1–19

    Article  Google Scholar 

  • Nichols E, Spector S, Louzada J, Larsen T, Amezquita S, Favila ME, The Scarabaeinae Research Network (2008) Ecological functions and ecosystem services provided by Scarabaeinae dung beetles. Biol Conserv 141:1461–1474

    Article  Google Scholar 

  • Noriega JA, Fagua G (2009) Monitoreo de escarabajos coprofagos (Coleoptera: Scarabaeidae) en la región neotropical. In: Técnicas de campo en ambientes tropicales. In: Acosta A, Fagua G, Zapata AM (eds) Manual para el monitoreo en ecosistemas acuáticos y artrópodos terrestres. Pontificia Universidad Javeriana, Bogotá, Colombia, pp 165–188

    Google Scholar 

  • Noriega JA, Botero JP, Viola M, Fagua G (2007) Dinámica estacional de la estructura trófica de un ensamblaje de Coleoptera en la Amazonía Colombiana. Rev Colomb Entomol 33(2):157–164

    Article  Google Scholar 

  • Noriega JA, Zapata-Prisco C, García H, Hernández E, Hernández J, Martínez R, Santos-Santos JH, Pablo-Cea JD, Calatayud J (2020) Does ecotourism impact biodiversity? An assessment using dung beetles (Coleoptera: Scarabaeinae) as bioindicators in a tropical dry forest natural park. Ecol Indic 117:106580

    Article  Google Scholar 

  • Oksanen J (2009) Ordination and analysis of dissimilarities: Tutorial with R and vegan, pp 1–25

  • Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2013) Vegan: community ecology package. R package version 2.0, p 7

  • Otavo S, Parrado-Rosselli A, Noriega JA (2013) Superfamilia Scarabaeoidea (Insecta: Coleoptera) como elemento bioindicador de perturbación antropogénica en un parque nacional amazónico. Rev Biol Trop 61:735–752

    Article  PubMed  Google Scholar 

  • Peres CA, Gardner TA, Barlow J, Zuanon J, Michalski F, Lees AC, Vieira ICG, Moreira FMS, Feeley KJ (2010) Biodiversity conservation in human-modified Amazonian forest landscapes. Biol Conserv 143:2314–2327

    Article  Google Scholar 

  • R Core Team (2016) R: a language and environment for statistical computing. R 707 Foundation for Statistical Computing, Vienna. http://www.r-project.org/

  • Ribeiro DB, Freitas AVL (2011) Large-sized insects show stronger seasonality than small-sized ones: a case study of fruit-feeding butterflies. Biol J Linn Soc 104:820–827

    Article  Google Scholar 

  • Rosenzweig ML (1995) Species diversity in space and time. Cambridge University Press, UK, p 436

    Book  Google Scholar 

  • Slade EM, Mann DJ, Villanueva JF, Lewis OT (2007) Experimental evidence for the effects of dung beetle functional group richness and composition on ecosystem function in a tropical forest. J Anim Ecol 76:1094–1104

    Article  PubMed  Google Scholar 

  • Tanner JE, Hughes TP, Connell JH (2009) Community-level density dependence: an example from a shallow coral assemblage. Ecology 90:506–516

    Article  PubMed  Google Scholar 

  • Tonelli M, Verdú JR, Zunino M (2018) Effects of the progressive abandonment of grazing on dung beetle biodiversity: body size matters. Biodivers Conserv 27:189–204

    Article  Google Scholar 

  • Tonelli M, Verdú JR, Morelli F, Zunino M (2020) Dung beetles: functional identity, not functional diversity, accounts for ecological process disruption caused by the use of veterinary medical products. J Insect Conserv 24:643–654

    Article  Google Scholar 

  • van Vliet N, Adams C, Vieira ICG, Mertz O (2013) “Slash and Burn” and “Shifting” cultivation systems in forest agriculture frontiers from the Brazilian Amazon. Soc Nat Resour 26:1454–1467

    Article  Google Scholar 

  • Vaz-de-Mello FZ, Edmonds WD, Ocampo FC, Schoolmeesters P (2011) A multilingual key to the genera and subgenera of the subfamily Scarabaeinae of the New World (Coleoptera: Scarabaeidae). Zootaxa 2854:1–73

    Article  Google Scholar 

  • Viega G, Stenert C, Schulz UH, Maltchik L (2014) Dung beetle communities as biological indicators of riparian forest widths in southern Brazil. Ecol Indic 36:703–710

    Article  Google Scholar 

  • Villéger S, Novack-Gottshall PM, Mouillot D (2011) The multidimensionality of the niche reveals functional diversity changes in benthic marine biotas across geological time. Ecol Lett 14:561–568

    Article  PubMed  Google Scholar 

  • Voss SC, Spafford H, Dadour IR (2009) Annual and seasonal patterns of insect succession on decomposing remains at two locations in Western Australia. Forest Sci Inter 193:26–36

    Article  Google Scholar 

  • Vulinec K (2002) Dung beetle communities and seed dispersal in primary forest and disturbed land in Amazonia. Biotropica 34:297–309

    Article  Google Scholar 

  • Walker LR, Del Moral R (2003) Primary succession and ecosystem rehabilitation. Cambridge University Press, Cambridge, UK, p 456

    Book  Google Scholar 

  • Wolda H (1988) Insect seasonality: why? Ann Rev Ecol Syst 19:1–18

    Article  Google Scholar 

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Acknowledgements

We thank the Faculty of Environmental Engineering of El Bosque University, the Palmari Natural Reserve, and its general manager Axel H. Antoine-Feill for helping with the logistics of field and laboratory work. To Jessica Veloza, Laura Alarcon, Eduardo Castaño, Laura Cifuentes, Felipe Cortes, Edgar Manosalva, Laura Martínez, Mery Tello, Lorena Velandia, and Andrés Vergara for their help during the field work in Palmari. To João Dos Santos, José Neris Da Silva Filho Bare, Franciney Pereira Tapudima “Maneu”, Carlos Acevedo Tapayuri “Maguila”, Francisco Hipolito Avila “Polo”, Ilke Coelho Ribeiro, and Kennedy López for their support and assistance in the Palmari Natural Reserve. To Giovanny Fagua and all the students of the Arthropods course of the Pontificia Javeriana University for their collaboration during the field and laboratory work in Monilla. To Juan Pablo Botero and Marcelo Viola for their valuable help in the cleaning, separation, and initial identification of the samples from Monilla. To Willson Teran and Pilar Marquez for the use of the analytical balance. To Fernando Vaz-de-Mello, David Edmonds, and Edgar Camero for their help in the species confirmation. And finally, to Lucía Maltez from English Syntax for her thorough English revision. This project was partly financed by the Faculty of Environmental Engineering of El Bosque University. JAN was supported by COLCIENCIAS-PDBC PhD scholarship No. 568 of 2012 (Colombia), and AMCS was supported by a ‘Juan de la Cierva’ Fellowship (IJCI-2014-19502) funded by the current Spanish Ministerio de Ciencia, Innovación y Universidades, and by the Portuguese Fundação para a Ciência e a Tecnología (contract CEEIND/03425/2017).

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Authors and Affiliations

  1. Departament of Biogeography & Global Change, Museo Nacional de Ciencias Naturales (MNCN-CSIC), C/José Gutiérrez Abascal 2, 28006, Madrid, Spain

    Jorge Ari Noriega, Joaquín Calatayud & Joaquín Hortal

  2. Laboratory of Zoology and Aquatic Ecology - LAZOEA, University of los Andes, Bogotá, Colombia

    Jorge Ari Noriega

  3. Global Change Ecology & Evolution (GLOCEE) Group, Department of Life Sciences, Universidad de Alcalá, Alcalá de Henares, Spain

    Ana M. C. Santos

  4. cE3c – Centre for Ecology Evolution and Environmental Changes, Faculdade de Ciências, Universidade de Lisboa, Lisboa, Portugal

    Ana M. C. Santos, Sergio Chozas & Joaquín Hortal

  5. Terrestrial Ecology Group (TEG-UAM), Departamento de Ecología, Facultad de Ciencias, Universidad Autónoma de Madrid, Madrid, Spain

    Ana M. C. Santos

  6. Centro de Investigación en Biodiversidad y Cambio Global (CIBC-UAM), Universidad Autónoma de Madrid, Madrid, Spain

    Ana M. C. Santos

  7. Area of Biodiversity and Conservation, Universidad Rey Juan Carlos, C/Tulipán s/n., 28933 Móstoles, Madrid, Spain

    Joaquín Calatayud

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  1. Jorge Ari Noriega
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  3. Joaquín Calatayud
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  4. Sergio Chozas
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  5. Joaquín Hortal
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Contributions

JAN originally formulated the idea, designed, and performed the samplings; JAN, AMCS, and JH designed research; JAN, AMCS, and JH designed the analyses, with JC and SC; JAN, JC, and SC analyzed the data; all authors interpreted results; JAN, AMCS, and JH wrote the paper; all authors approved the final version of the manuscript.

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Correspondence to Jorge Ari Noriega.

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Communicated by Liliane Ruess.

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Noriega, J.A., Santos, A.M.C., Calatayud, J. et al. Short- and long-term temporal changes in the assemblage structure of Amazonian dung beetles. Oecologia 195, 719–736 (2021). https://doi.org/10.1007/s00442-020-04831-5

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  • DOI: https://doi.org/10.1007/s00442-020-04831-5

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