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
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
Andresen E (2002) Dung beetles in a Central Amazonian rainforest and their ecological role as secondary seed dispersers. Ecol Entomol 27:257–270
Andresen E (2005) Effects of season and vegetation type on community organization of dung beetles in a tropical dry forest. Biotropica 37:291–300
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
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
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
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
Baselga A (2010) Partitioning the turnover and nestedness components of beta diversity. Global Ecol Biogeogr 19:134–143
Baselga A, Orme CDL (2012) betapart: an R package for the study of beta diversity. Met Ecol Evol 3:808–812
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
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
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
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
Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New York, p 488
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
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
Camero E (2010) Los escarabajos del género Eurysternus Dalman, 1824 (Coleoptera: Scarabaeidae) de Colombia. Bol Soc Entomol Arag 46:147–179
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
Cook J (2002) A revision of the neotropical genus Cryptocanthon. Coleopt Soc Monogr 1:1–96
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
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
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
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
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
Denslow JS (1980) Patterns of plant species diversity during succession under different disturbance regimes. Oecologia 46:18–21
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
Doube B (1990) A functional classification for analysis of the structure of dung beetle assemblages. Ecol Entomol 15:371–383
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
Edmonds WD, Zídek J (2004) Revision of the Neotropical dung beetle genus Oxysternon (Scarabaeidae: Scarabaeinae: Phanaeini). Folia Heyrovskyana Suppl 11:1–58
Edmonds WD, Zídek J (2010) A taxonomic review of the neotropical genus Coprophanaeus Olsoufieff, 1924 (Coleoptera: Scarabaeidae, Scarabaeinae). Insect Mundi 0129:1–111
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
Encinas-Viso F, Revilla TA, Etienne RS (2012) Phenology drives mutualistic network structure and diversity. Ecol Lett 15:198–208
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
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
Feer F, Boissier O (2015) Variations in dung beetle assemblages across a gradient of hunting in a tropical forest. Ecol Ind 57:164–170
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
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
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
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
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
Genier F (1996) A revision of the neotropical genus Ontherus Erichson (Coleoptera: Scarabaeidae, Scarabaeinae). Mem Entomol Soc Canada 170:1–168
Gleason HA (1927) Further views on the succession concept. Ecology 8:299–326
Grimbacher PS, Stork NE (2009) Seasonality of a diverse beetle assemblage inhabiting lowland tropical rain forest in Australia. Biotropica 41:328–337
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
Halffter G, Arellano L (2002) Response of dung beetle diversity to human-induced changes in a tropical landscape. Biotropica 34:144–154
Halffter G, Edmonds WD (1982) The nesting behaviour of dung beetles (Scarabaeinae): an ecological and evolutive approach. Instituto de Ecología, MAB-UNESCO, México, DF
Halffter G, Matthews EG (1966) The natural history of dung beetles of the subfamily Scarabaeinae. Folia Entomol Mex 12–14:1–312
Hanski I (1982) Dynamics of regional distribution: the core and satellite species hypothesis. Oikos 38:210–221
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
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
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
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
Horgan FG (2008) Dung beetle assemblages in forests and pastures of El Salvador: a functional comparison. Biodiv Conserv 17:2961–2978
Hortal J, De Marco P, Santos AMC, Diniz-Filho AF (2012) Integrating biogeographical processes and local community assembly. J Biogeogr 39:627–628
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
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
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
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
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
Larsen TH, Forsyth A (2005) Trap spacing and transect design for dung beetle biodiversity studies. Biotropica 37:322–325
Lenth RV (2016) Least-squares means: The R package lsmeans. J Stat Softw 69(1):1–33
Lobo JM (2001) Decline of roller dung beetle (Scarabaeinae) populations in the Iberian península during the 20th century. Biol Conserv 97:43–50
Lobo JM (2008) Database records as a surrogate for sampling effort provide higher species richness estimations. Biodiv Conserv 17:873–881
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
Losey JE, Vaughan M (2006) The economic value of ecological services provided by insects. Bioscience 56:311–323
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
McCune B, Grace JB (2002) Analysis of ecological communities. MjM software design, Gleneden Beach, Oregon
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
Menéndez R (1994) Patrones de distribución y abundancia en especies de escarabajos coprófagos. Stvdia Oecol 10–11:395–400
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
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
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
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
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
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
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
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
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
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
Rosenzweig ML (1995) Species diversity in space and time. Cambridge University Press, UK, p 436
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
Tanner JE, Hughes TP, Connell JH (2009) Community-level density dependence: an example from a shallow coral assemblage. Ecology 90:506–516
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
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
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
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
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
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
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
Vulinec K (2002) Dung beetle communities and seed dispersal in primary forest and disturbed land in Amazonia. Biotropica 34:297–309
Walker LR, Del Moral R (2003) Primary succession and ecosystem rehabilitation. Cambridge University Press, Cambridge, UK, p 456
Wolda H (1988) Insect seasonality: why? Ann Rev Ecol Syst 19:1–18
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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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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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