A comparison of dung beetle assemblages (Coleoptera, Scarabaeoidea) collected 34 years apart in an Iberian mountain locality

  • Eva Cuesta
  • Jorge M. LoboEmail author


Knowing how recent environmental changes may have affected species diversity is a major objective to estimate the consequences of habitat alteration and climate change. In this study two dung beetle inventories made in the same locality of the Sierra de Guadarrama (Madrid, Spain) 34 years apart (1983–2017) are compared. Changes in diversity, species richness, abundances and composition were analysed and species replacements described considering the three main functional dung beetle groups: large paracoprids, small paracoprids and small endocoprids. In addition, changes in vegetation cover and climate between the two periods were also analysed to examine their association with the detected faunistic changes. Both the vegetation and climatic data show that the surveyed locality would have experienced an increase in the area covered by bushes and forest and an increase in temperature and warm conditions during the 34 years. These changes are associated with a probable increase in species richness and species dominance, a decrease in diversity and an important change in composition that would have positively affected small paracoprids but negatively affected large paracoprids.


Sierra de Guadarrama Intertemporal variation Climate change Land use change Chao estimator 



This work was supported by the MINECO-FEDER Project CGL2015-64489-P and the MINECO-FEDER Contract BES-2016-077087 granted to the first author. We are indebted to Luis María Carrascal for his valuable suggestions.

Compliance with ethical standards

Conflict of interest

There is no conflict of interest that could be perceived to bias the work.

Ethical approval

Beetle collection was conducted with relevant permissions provided by the Comunidad de Madrid (Dirección General de Medio Ambiente), considering all applicable international and national guidelines for the care and use of animals.


  1. Agoglitta R, Moreno CE, Rossini M, Tonelli M, Zunino M (2012) Variación temporal en la diversidad y composición de una comunidad coprófila del euromediterráneo (Coleoptera: Scarabaeoidea). Interciencia 37:44–48Google Scholar
  2. Arroyo P, Cifuentes N, Grande MA, Martín MA (1993) La ordenación ganadera en sistemas rurales en crisis. El caso de los términos municipales de Cercedilla y Navacerrada. Congreso Forestal Español 4:149–152Google Scholar
  3. Ashton LA, Barlow HS, Nakamura A, Kitching RL, Didham R (2015) Diversity in tropical ecosystems: the species richness and turnover of moths in Malaysian rainforests. Insect Conserv Diver 8:132–142. CrossRefGoogle Scholar
  4. Beiroz W, Slade EM, Barlow J, Silveira JM, Louzada J, Sayer E (2017) Dung beetle community dynamics in undisturbed tropical forest: implications for ecological evaluations of land –use change. Insect Conserv Diver 10:94–106. CrossRefGoogle Scholar
  5. Benton TG, Bryant DM, Cole L, Crick HQ (2002) Linking agricultural practice to insect and bird populations: a historical study over three decades. J Appl Ecol 39:673–687. CrossRefGoogle Scholar
  6. Birkett AJ, Blackburn GA, Menéndez R (2018) Linking species thermal tolerance to elevational range shifts in upland dung beetles. Ecography 41:1–10. CrossRefGoogle Scholar
  7. Chao A, Jost L (2012) Coverage-based rarefaction and extrapolation: Standardizing samples by completeness rather than size. Ecology 93:2533–2547. CrossRefGoogle Scholar
  8. Chao A, Jost L (2015) Estimating diversity and entropy profiles via discovery rates of new species. Methods Ecol Evol 6:873–882. CrossRefGoogle Scholar
  9. Chao A, Wang YT, Jost L (2013) Entropy and the species accumulation curve: a novel entropy estimator via discovery rates of new species. Methods Ecol Evol 4:1091–1100. CrossRefGoogle Scholar
  10. Chao A, Colwell RK, Chiu CH, Townsend D (2017) Seen once or more than once: applying good-turing theory to estimate species richness using only unique observations and a species list. Methods Ecol Evol 8:1221–1232. CrossRefGoogle Scholar
  11. Conrad KF, Woiwod IP, Perry JN (2002) Long-term decline in abundance and distribution of the garden tiger moth (Arctia caja) in Great Britain. Biol Conserv 106:329–337. CrossRefGoogle Scholar
  12. Davis ALV (1997) Climatic and biogeographical associations of southern African dung beetles (Coleoptera: Scarabaeidae s. str.). Afr J Ecol 35:10–38CrossRefGoogle Scholar
  13. Dirzo R, Young HS, Galetti M, Ceballos G, Isaac NJ, Collen B (2015) Defaunation in the anthropocene. Science 345:401–406. CrossRefGoogle Scholar
  14. Dortel E, Thuiller W, Lobo JM, Bohbot H, Lumaret JP, Jay-Robert P (2013) Potential effects of climate change on the distribution of Scarabaeidae dung beetles in Western Europe. J Insect Conserv 17:1059–1070. CrossRefGoogle Scholar
  15. Ellwood ER, Diez JM, Ibáñez I, Primack RB, Kobori H, Higuchi H, Silander JA (2012) Disentangling the paradox of insect phenology: are temporal trends reflecting the response to warming? Oecologia 168:1161–1171. CrossRefGoogle Scholar
  16. Escobar F, Halffter G, Solís Á, Halffter V, Navarrete D (2008) Temporal shifts in dung beetle community structure within a protected area of tropical wet forest: a 35-year study and its implications for long-term conservation. J Appl Ecol 45:1584–1592. CrossRefGoogle Scholar
  17. Fox R, Oliver TH, Harrower C, Parsons MS, Thomas CD, Roy DB (2014) Long-term changes to the frequency of occurrence of British moths are consistent with opposing and synergistic effects of climate and landuse changes. J Appl Ecol 51:949–957. CrossRefGoogle Scholar
  18. Halffter G, Arellano L (2002) Response of dung beetle diversity to human-induced changes in a tropical landscape. Biotropica 34:144–154CrossRefGoogle Scholar
  19. Hallmann CA, Sorg M, Jongejans E, Siepel H, Hofland N, Schwan H, Stenmans W, Muller A, Sumser H, Horren T, Goulson D, Kroon H (2017) More than 75 percent decline over 27 years in total flying insect biomass in protected areas. PLoS ONE 12.
  20. Hanski I, Cambefort Y (1991) Resource partitioning. In: Hanski I, Cambefort Y (eds) Dung beetle ecology. Princeton University Press, Princeton, pp 330–349Google Scholar
  21. Hortal J, Martín-Piera F, Lobo JM (2000) Dung beetle geographic diversity variation along a western Iberian latitudinal transect (Col., Scarabaeidae). Ann Entomol Soc Am 93:235–243.CrossRefGoogle Scholar
  22. Howden HF, Howden AT (2001) Change through time: a third survey of the Scarabaeinae (Coleoptera:Scarabaeidae) at Welder Wildlife Refuge. Coleopt Bull 55:356–362.CrossRefGoogle Scholar
  23. Howden HF, Scholtz CH (1986) Changes in a Texas dung beetle community between 1975 and 1985 (Coleoptera: Scarabaeidae, Scarabaeinae). Coleopt Bull 40:313–316Google Scholar
  24. Hsieh TC, Ma KH, Chao A (2016) iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods Ecol Evol 7:1451–1456. CrossRefGoogle Scholar
  25. Jost L (2007) Partitioning diversity into independent alpha and beta components. Ecology 88:2427–2439. CrossRefGoogle Scholar
  26. Lane SA, Mann DJ (2016) A review of the status of the beetles of Great Britain: the stag beetles, dor beetles, dung beetles, chafers and their allies-Lucanidae. Geotrupidae, Trogidae and Scarabaeidae. Natural England Comissioned Report NECR224Google Scholar
  27. Lobo JM (2001) Decline of roller dung beetle (Scarabaeinae) populations in the Iberian Peninsula during the 20th century. Biol Conserv 97:43–50. CrossRefGoogle Scholar
  28. Lobo JM, Morón MA (1993) La modificación de las comunidades de coleópteros Melolonthidae y Scarabaeidae en dos áreas protegidas mexicanas tras dos décadas de estudios faunísticos. G it Ent 6:391–406Google Scholar
  29. Lobo JM, Martín-Piera F, Veiga CM (1988) Las trampas pitfall con cebo, sus posibilidades en el estudio de las comunidades coprófagas de Scarabaeoidea (Col.) I. Características determinantes de su capacidad de captura. Rev Ecol Biol Sol 25:77–100Google Scholar
  30. Loboda S, Savage J, Buddle CM, Schmidt NM, Høye TT (2018) Declining diversity and abundance of High Arctic fly assemblages over two decades of rapid climate warming. Ecography 41:265–277. CrossRefGoogle Scholar
  31. Lumaret JP, Kadiri N, Bertrand M (1992) Changes in resources: consequences from the dynamics of dung beetle communities. J Appl Ecol 29:349–356CrossRefGoogle Scholar
  32. Martín-Piera F, López-Colón JI (2000) Coleoptera. Scarabaeoidea I. Fauna Ibérica, vol 14. Museo Nacional de Ciencias Naturales, CSIC, MadridGoogle Scholar
  33. Martín-Piera F, Veiga CM, Lobo JM (1992) Ecology and biogeography of dung-beetle communities (Coleoptera, Scarabaeoidea) in an Iberian mountain range. J Biogeogr 19:677–691CrossRefGoogle Scholar
  34. Menéndez R (2007) How are insects responding to global warming? Tijdschr Entomol 150:355–365Google Scholar
  35. Menéndez R, Gutiérrez D (2004) Shifts in habitat associations of dung beetles in northern Spain: climate change implications. Ecoscience 11:329–337. CrossRefGoogle Scholar
  36. Menéndez R, González-Megías A, Jay-Robert P, Marquéz-Ferrando R (2014) Climate change and elevational range shifts: evidence from dung beetles in two European mountain ranges. Glob Ecol Biogeogr 23:646–657. CrossRefGoogle Scholar
  37. Nichols E, Spector S, Louzada J, Larsen T, Amezquita S, Favila ME (2008) Ecological functions and ecosystem services provided by Scarabaeinae dung beetles. Biol Conserv 141:461–1474. Google Scholar
  38. Nieto-Sánchez S, Gutiérrez D, Wilson RJ (2015) Long-term change and spatial variation in butterfly communities over an elevational gradient: driven by climate, buffered by habitat. Divers Distrib 21:950–961. CrossRefGoogle Scholar
  39. Rivas-Martínez S (1982) Memoria del mapa de las series de vegetación de la provincia de Madrid (1:200.000). Diputación de Madrid, Servicio Forestal y Medio AmbienteGoogle Scholar
  40. Sanz-Elorza M, Dana ED, González A, Sobrino E (2003) Changes in the high-mountain vegetation of the central Iberian Peninsula as a probable sign of global warming. Ann Bot 92:273–280. CrossRefGoogle Scholar
  41. Sprent P, Smeeton NC (2007) Applied nonparametric statistical methods. CRC Press, Boca RatonGoogle Scholar
  42. Thomas JA (2016) Butterfly communities under threat. Science 353:216–218. CrossRefGoogle Scholar
  43. Tobin PC, Nagarkatti S, Loeb G, Saunders MC (2008) Historical and projected interactions between climate change and insect voltinism in a multivoltine species. Glob Chang Biol 14:951–957. CrossRefGoogle Scholar
  44. Touroult J, Dalens PH, Giuglaris JL, Lapèze J, Boilly O (2017) Structure des communautés de Phanaeini (Coleoptera: Scarabaeidae) de Guyane: étude par échantillonnage massif au piège d’interception (N.S.). Ann Soc Entomol Fr 53:143–161. CrossRefGoogle Scholar
  45. Veiga CM (1998) Los Aphodiinae (Coleoptera, Aphodiidae) ibéricos. Tesis Doctoral. Universidad Complutense de Madrid. MadridGoogle Scholar
  46. Veiga CM, Lobo JM, Martín-Piera F (1989) Las trampas pitfall con cebo, sus posibilidades en el estudio de las comunidades coprófagas de Scarabaeoidea (Col.) II. Análisis de efectividad. Rev Ecol Biol Sol 26:91–109Google Scholar
  47. Verdú JR, Lobo JM, Sánchez-Piñero F, Gallego B, Numa C, Lumaret JP, Cortez V, Ortiz AJ, Tonelli M, García-Teba JP, Rey A, Rodríguez A, Durán J (2018) Ivermectin residues disrupt dung beetle diversity, soil properties and ecosystem functioning: an interdisciplinary field study. Sci Total Environ 618:219–228. CrossRefGoogle Scholar
  48. Wilson RJ, Gutiérrez D, Gutiérrez J, Martínez D, Agudo R, Monserrat VJ (2005) Changes to the elevational limits and extent of species ranges associated with climate change. Ecol Lett 8:1138–1146. CrossRefGoogle Scholar
  49. Wilson RJ, Gutiérrez D, Gutiérrez J, Monserrat VJ (2007) An elevational shift in butterfly species richness and composition accompanying recent climate change. Glob Chang Biol 13:1873–1887. CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Dpto. Biogeografía y Cambio GlobalMuseo Nacional de Ciencias Naturales, (C.S.I.C)MadridSpain
  2. 2.Escuela Internacional de DoctoradoUniversidad Rey Juan CarlosMóstoles (Madrid)Spain

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