Respuesta de los escarabajos carroñeros Nicrophorus olidus y Oxelytrum discicolle (Coleoptera: Silphidae) a la restauración activa y pasiva en un paisaje de bosque de niebla en México
DOI:
https://doi.org/10.22201/ib.20078706e.2023.94.5162Palabras clave:
Abundancia, Dinámica de poblaciones, Éxito de restauración, Recuperación de faunaResumen
La restauración activa y la restauración pasiva son estrategias utilizadas para recuperar paisajes forestales. Pocos estudios han evaluado la recuperación de la fauna comparando diferentes estrategias de restauración de la misma edad en un paisaje tropical. En este estudio comparamos la abundancia y la frecuencia de presencia de los escarabajos carroñeros Nicrophorus olidus y Oxelytrum discicolle, entre un bosque en restauración pasiva de 23 años (RP), un bosque en restauración activa de 23 años (RA), un pastizal ganadero y un bosque de niebla. Analizamos cómo varían las poblaciones de los escarabajos entre temporadas climáticas y examinamos la relación de 10 variables del hábitat con la respuesta de los escarabajos. Nicrophorus olidus fue más abundante en RA y O. discicolle en RP. La abundancia de ambas especies varió entre temporadas. La respuesta de N. olidus a la restauración estuvo relacionada con las coberturas del dosel y del helecho Pteridium arachnoideum. La abundancia de O. discicolle no estuvo relacionada con ninguna variable. Cada estrategia de restauración ofrece condiciones ambientales que influyen de manera diferencial en las especies, aun cuando pertenecen al mismo gremio. Destacamos la importancia de restaurar paisajes con estrategias complementarias que contribuyan a recuperar poblaciones de distintas especies.
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Anderson, R. S. (1982). Resource partitioning in the carrion beetle (Coleoptera: Silphidae) fauna of southern Ontario: ecological and evolutionary considerations. Canadian Journal of Zoology, 60, 1314–1325. https://doi.org/10.1139/z82-178
Arellano, L., Favila, M. E. y Huerta, C. (2005). Diversity of dung and carrion beetles in a disturbed Mexican tropical montane cloud forest and on shade coffee plantations. Biodiversity and Conservation, 14, 601–615. https://doi.org/10.1007/s10531-004-3918-3
Audino, L. D., Louzada, J. y Comita, L. (2014). Dung beetles as indicators of tropical forest restoration success: is it possible to recover species and functional diversity? Biological Conservation, 169, 248–257. https://doi.org/10.1016/j.biocon.2013.11.023
Carvalho, L. M., Thyssen, P. J., Linhares, A. X. F. y Palhares, A. B. (2000). A checklist of arthropods associated with pig carrion and human corpses in Southeastern Brazil. Memórias do Instituto Oswaldo Cruz, 95, 135–138. https://doi.org/10.1590/S0074-02762000000100023
Catterall, C. P. (2018). Fauna as passengers and drivers in vegetation restoration: a synthesis of processes and evidence. Ecological Management and Restoration, 19, 54–62. https://doi.org/10.1111/emr.12306
Cole, R. J., Holl, K. D., Zahawi, R. A., Wickey, P. y Townsend, A. R. (2016). Leaf litter arthropod responses to tropical forest restoration. Ecology and Evolution, 6, 5158–5168. https://doi.org/10.1002/ece3.2220
Conabio (Comisión Nacional para el Conocimiento y Uso de la Biodiversidad). (2010). El bosque mesófilo de montaña en México: amenazas y oportunidades para su conservación y manejo sostenible. México D.F.: Conabio.
Conagua (Comisión Nacional del Agua). (2016). Estaciones Meteorológicas Automáticas, Los Tuxtlas II. Servicio Meteorológico Nacional. Recuperado el 06 mayo, 2023 de: https://smn.conagua.gob.mx/
Cross, S. L., Bateman, P. W. y Cross, A. T. (2019). Restoration goals: Why are fauna still overlooked in the process of recovering functioning ecosystems and what can be done about it? Ecological Management and Restoration, 21, 4–8. https://doi.org/10.1111/emr.12393
Crouzeilles, R., Ferreira, M. S., Chazdon, R. L., Lindenmayer, D. B., Sansevero, J. B. B., Monteiro, L. et al. (2017). Ecological restoration success is higher for natural regeneration than for active restoration in tropical forests. Science Advances, 3, 1–7. https://doi.org/10.1126/sciadv.1701345
Deloya, C., Parra-Tabla, V. y Delfín-González, H. (2007). Fauna de Coleópteros Scarabaeidae Laparosticti y Trogidae (Coleoptera: Scarabaeoidea) asociados al bosque mesófilo de montaña, cafetales bajo sombra y comunidades derivadas en el centro de Veracruz, México. Neotropical Entomology, 36, 5–21. https://doi.org/10.1590/S1519-566X2007000100002
Díaz-García, J. M., López-Barrera, F., Toledo-Aceves, T., Andresen, E. y Pineda, E. (2020). Does forest restoration assist the recovery of threatened species? A study of cloud forest amphibian communities. Biological Conservation, 242, 108400. https://doi.org/10.1016/j.biocon.2019.108400
Díaz-García, J. M., Pineda, E., López-Barrera, F., Moreno, C. E. (2017). Amphibian species and functional diversity as indicators of restoration success in tropical montane forest. Biodiversity and Conservation, 26, 2569–2589. https://doi.org/10.1007/s10531-017-1372-2
Dixon, K. W. (2009). Pollination and restoration. Science, 325, 571–573. https://doi.org/10.1126/science.1176295
Fagan, M. E., Reid, J. L., Holland, M. B., Drew, J. D. y Zahawi, R. A. (2020). How feasible are global forest restoration commitments? Conservation Letters, 13, 1–8. https://doi.org/10.1111/conl.12700
Fife, D. A. (2014). An introduction to the fifer package in R. Recuperado el 20 marzo, 2023 de: https://CRAN.R-project.org/package=fifer
Fraser, L. H., Harrower, W. L., Garris, H. W., Davidson, S., Hebert, P. D. N., Howie, R. et al. (2015). A call for applying trophic structure in ecological restoration. Restoration Ecology, 23, 503–507. https://doi.org/10.1111/rec.12225
Gann, G. D., McDonald, T., Walder, B., Aronson, J., Nelson, C. R., Johnson, J. et al. (2019). International principles and standards for the practice of ecological restoration. Restoration Ecology, 27, 1–46. https://doi.org/10.1111/rec.13035
Gibbs, J. P. y Stanton, E. J. (2001). Habitat fragmentation and arthropod community change: carrion beetles, phoretic mites, and flies. Ecological Applications, 11, 79–85. https://doi.org/10.1890/1051-0761(2001)011[0079:HFAACC]2.0.CO;2
Gilman, A. C., Letcher, S. G., Fincher, R. M., Pérez, A. I., Madell, T. W., Finkelstein, A. L. et al. (2016). Recovery of floristic diversity and basal area in natural forest regeneration and planted plots in a Costa Rican wet forest. Biotropica, 48, 798–808. https://doi.org/10.1111/btp.12361
Google Earth (2019). Imagen de Huatusco, Veracruz, México. Google Earth. Recuperado el 20 marzo, 2023 de: https://n9.cl/igdr6
Guariguata, M. R. y Ostertag, R. (2001). Neotropical secondary forest succession: changes in structural and structural and functional characteristics. Forest Ecology and Management, 148, 185–206. https://doi.org/10.1016/S0378-1127(00)00535-1
Halffter, G., Favila, M. E. y Arellano, L. (1995). Spatial distribution of three groups of Coleoptera along an altitudinal transect in the Mexican Transition Zone and its biogeographical implications. Elytron, 9, 151–185.
Harmon, L. J., Jason, T. W., Chad, D. B., Richard, E. G. y Challenger, W. (2008). GEIGER: investigating evolutionary radiations. Bioinformatics, 24, 129–131. https://doi.org/10.1093/bioinformatics/btm538
Holloway, A. K. y Schnell, G. D. (1997). Relationship between numbers of the endangered American burying beetle Nicrophorus americanus (Coleoptera: Silphidae) and available food resources. Biological Conservation, 81, 145–152. https://doi.org/10.1016/S0006-3207(96)00158-9
Kalinová, B., Podskalská, H., Růžička, J. y Hoskovec, M. (2009) Irresistible bouquet of death - how are burying beetles (Coleoptera: Silphidae: Nicrophorus) attracted by carcasses. Naturwissenschaften, 96, 889–899. https://doi.org/10.1007/s00114-009-0545-6
Kanowski, J., Catterrall, C. P., Proctor, H., Reis, T., Tucker, N. y Wardell-Johnson, G. (2005). Biodiversity values of timber plantations and restoration plantings for rainforest fauna in tropical and subtropical Australia. En P. Erskine, D. Lamb, M. Bristow (Eds.), Reforestation in the tropics and subtropics of Australia using rainforest tree species (pp. 183–205). Canberra, Australia: Rainforest Cooperative Research Center.
Kattan, G. H., Correa, D., Escobar, F. y Medina, C. (2006). Leaf-litter arthropods in restored forests in the Colombian Andes: a comparison between secondary forest and tree plantations. Restoration Ecology, 14, 95–102. https://doi.org/10.1111/j.1526-100X.2006.00109.x
Korhonen, L., Korhonen, K. T., Rautiainen, M. y Stenberg, P. (2006). Estimation of forest canopy cover: comparison of field measurement techniques. Silva Fennica, 40, 577–588. https://doi.org/10.14214/sf.315
Lanping, L., Cadotte, M. W., Martínez-García, C. y de la Peña-Domene, M. (2017). Planting accelerates restoration of tropical forest but assembly mechanisms appear insensitive to initial composition. Journal of Applied Ecology, 55, 986–996. https://doi.org/10.1111/1365-2664.12976
Lawes, M. J., Moore, A. M., Andersen, A. N., Preece, N. D. y Franklin, C. D. (2017). Ants as ecological indicators of rainforests restoration: community convergence and the development of an Ant Forest Indicator Index in the Australian wet tropics. Ecology and Evolution, 7, 8442–8455. https://doi.org/10.1002/ece3.2992
Lira, L. A. y Vasconcelos, S. D. (2016). New Record and Update on the Distribution of Oxelytrum discicolle (Brullé, 1840) (Coleoptera: Silphidae) in South America. The Coleopterists Bulletin, 70, 399–402. https://doi.org/10.1649/0010-065X-70.2.399
Lomolino, M. V. y Creighton, J. C. (1996). Habitat selection, breeding success and conservation of the endangered American burying beetle Nicrophorus americanus. Biological Conservation, 77, 235–241. https://doi.org/10.1016/0006-3207(96)00003-1
Lowe, A. J. y Lauff, R. F. (2015). Habitat and microhabitat preferences in a Nova Scotian carrion beetle (Coleoptera: Silphidae) community. En O. R. P. Bininda-Emonds, G. L. Powell, H. A. Jamniczky, A. M. Bauer y J. Theodor (Eds.). All animals are interesting: a festschrift in honour of Anthony P. Russell (pp. 455–468). Oldenburg, Alemania: BIS Verlag.
MacArthur, R. y Levins, R. (1964). Competition, habitat selection, and character displacement in a patchy environment. Proceedings of the National Academy of Sciences, 51, 1207–1210. https://doi.org/10.1073/pnas.51.6.1207
Majer, J. D. (2009). Animals in the restoration process - progressing the trends. Restoration Ecology, 17, 315–319. https://doi.org/10.1111/j.1526-100X.2009.00528.x
Martín-Vega, D. y Baz, A. (2012). Spatiotemporal distribution of necrophagous beetles (Coleoptera: Dermestidae, Silphidae) assemblages in natural habitats of central Spain. Annals of the Entomology Society of America, 105, 44–53. https://doi.org/10.1603/AN11062
Meli, P., Holl, K. D., Rey-Benayas, J. M., Jones, H. P., Jones, P. C., Montoya, D. et al. (2017). A global review of past land use, climate, and active vs passive restoration effects on forest recovery. Plos One, 12, e0171368. https://doi.org/10.1371/journal.pone.0171368
Merrick, M. J., y Smith, R. J. (2004). Temperature regulation in burying beetles (Nicrophorus spp.: Coleoptera: Silphidae): effects of body size, morphology and environmental temperature. Journal of Experimental Biology, 207, 723–733. https://doi.org/10.1242/jeb.00807
Morrison, E. B. y Lindell, C. A. (2011). Active or passive forest restoration? Assessing restoration alternatives with avian foraging behavior. Restoration Ecology, 19, 170–177. https://doi.org/10.1111/j.1526-100X.2010.00725.x
Naranjo-López, A. G. y Navarrete-Heredia, J. L. (2011). Coleópteros necrócolos (Histeridae, Silphidae y Scarabaeidae) en dos localidades de Gómez Farías, Jalisco, México. Revista Colombiana de Entomología, 37, 103–110. https://doi.org/10.25100/socolen.v37i1.9051
Navarrete-Heredia, J. L. (1995). Coleópteros Silphidae de Jalisco y del volcán de Tequila incluyendo comentarios generales sobre su biología. Dugesiana, 26, 11–28.
Navarrete-Heredia, J. L. (2009). Silphidae (Coleoptera) de México: diversidad y distribución. Guadalajara, Jalisco: Universidad de Guadalajara.
Peck, S. B. y Anderson, R. S. (1985). Taxonomy, phylogeny and biogeography of the carrion beetles of Latin America (Coleoptera: Silphidae). Quaestiones Entomologicae, 21, 243–317.
Pérez-Gracida, L. D. (2021). Características de la comunidad de mamíferos en un área restaurada y un fragmento de bosque mesófilo de montaña, Huatusco, Veracruz, México (Tesis). Facultad de Ciencias Biológicas Agropecuarias Región Orizaba-Córdoba. Universidad Veracruzana. Peñuela, Veracruz.
Pérez-Villamares, J. C., Jiménez-Sánchez, E. y Padilla-Ramírez, J. (2016). Escarabajos atraídos a la carroña (Coleoptera: Scarabaeidae, Geotrupidae, Hybosoridae, Trogidae y Silphidae) en las cañadas de Coatepec Harinas, Estado de México, México. Revista Mexicana de Biodiversidad, 87, 443–450. https://doi.org/10.1016/j.rmb.2016.03.005
Quiroz-Rocha, G. A., Navarrete-Heredia, J. L. y Martínez, P. (2008). Especies de Scarabaeinae (Coleoptera: Scarabaeidae) y Silphidae (Coleoptera) necrófilas de bosque de pino-encino y bosque mesófilo de montaña en el municipio de Mascota, Jalisco, México. Dugesiana, 15, 27–37.
R Core Team, (2017). A Language and Environment for Statistical Computing. Recuperado el 20 marzo, 2023 de: https://www.R-project.org/
Ramírez-Soto, A., Lucio-Palacio, C. R., Rodríguez-Mesa, R., Sheseña-Hernández, I., Farhat, F. N., Villa-Bonilla, B. et al. (2018). Restoration of tropical montane cloud forests: a six-prong strategy. Restoration Ecology, 26, 106–211. https://doi.org/10.1111/rec.12660
Ratcliffe, B. C. (1996). The carrion beetles (Coleoptera: Silphidae) of Nebraska. Lincoln: University of Nebraska.
Rivera-Cervantes, L. E. y García-Real, E. (1998). Análisis preliminar sobre la composición de los escarabajos necrófilos (Coleoptera: Silphidae y Scarabaeidae) presentes en dos bosques de pino (uno dañado por fuego), en la estación científica Las Joyas, Sierra de Manantlán, Jalisco, México. Dugesiana, 5, 11–22.
Romero-González, R. (2018). Ganadería agroecológica en una zona de bosque de niebla. En G. Halffter, M. Cruz y C. Huerta (Eds.), Ganadería sustentable en el golfo de México (pp. 345–367). Xalapa, México: Instituto de Ecología, A.C.
Scott, M. P. (1998). The ecology and behavior of burying beetles. Annual Review of Entomology, 43, 595–618. https://doi.org/10.1146/annurev.ento.43.1.595
Schwartz, M. B. y Salisbury, N. (2018). The native pollinator habitat restoration guide. Washington D.C.: Earth Cops.
Shoo, L. P., Freebody, K., Kanowski, J. y Catterall, C. P. (2016). Slow recovery of tropical old-field rainforest regrowth and the value and limitations of active restoration. Conservation Biology, 30, 121–132. https://doi.org/10.1111/cobi.12606
Smith, G. C., Lewis, T. y Hogan L. D. (2015). Fauna community trends during early restoration of alluvial open forest/woodland ecosystems on former agricultural land. Restoration Ecology, 23, 787–799. https://doi.org/10.1111/rec.12269
Suganuma, M. S., de Assis, G. B. y Durigan, G. (2014). Changes in plant species composition and functional traits along the successional trajectory of a restored patch of Atlantic Forest. Community Ecology, 15, 27–36. https://doi.org/10.1556/ComEc.15.2014.1.3
Trevilla-Rebollar, A., Deloya, C. y Padilla-Ramírez, J. (2010). Coleópteros necrófilos (Scarabaeidae, Silphidae y Trogidae) de Malinalco, Estado de México, México. Neotropical Entomology, 39, 486–495. https://doi.org/10.1590/S1519-566X2010000400005
Trujillo-Miranda, A. L., Toledo-Aceves, T., López-Barrera, F. y Gerez-Fernández, P. (2018). Active versus passive restoration: recovery of cloud forest structure, diversity and soil condition in abandoned pastures. Ecological Engineering, 117, 50–61. https://doi.org/10.1016/j.ecoleng.2018.03.011
Trumbo, S. T. (1990). Reproductive success, phenology and biogeography of burying beetles (Silphidae, Nicrophorus). The American Midland Naturalist, 124, 1-11. https://doi.org/10.2307/2426074
van Klink, R., Bowler, D. E., Gongalsky, K. B., Swengel, A. B., Gentile, A. y Chase, J. M. (2020). Meta-analysis reveals declines in terrestrial but increases in freshwater insect abundances. Science, 368, 417–420. https://doi.org/10.1126/science.aax9931
von Hoermann, C., Jauch, D., Kubotsh, C., Reichel-Jung, K., Steiger, S. y Ayasse, M. (2018). Effects of abiotic environmental factors and land use on the diversity of carrion-visiting silphid beetles (Coleoptera: Silphidae): a large scale carrion study. Plos One, 13, e0196839. https://doi.org/10.1371/journal.pone.0196839
Venables, W. N. y Ripley, B. D. (2002). Modern applied statistics with S. New York: Springer. https://doi.org/10.1007/978-0-387-21706-2
Warnes, G. R., Bolker, B., Lumley, T. y Johnson, R. C. (2018). gmodels: various R Programming tools for model fitting for R. Recuperado el 20 marzo, 2023 de: https://cran.r-project.org/web/packages/gmodels/index.html
WRI. (2019). The world lost a Belgium-sized area of primary rainforests last year. https://www.wri.org/blog/2019/04/world-lost-belgium-sized-area-primary-rainforests-lastyear, Recuperado el 10 de junio de 2020.
