The role of dung beetles in seed dispersal in an arid environment

M. Belén Maldonado; Alejandro M. Serrano; Natacha P. Chacoff; Diego P. Vazquez

doi:10.25260/EA.23.33.2.0.2075

Autores/as

M. Belén Maldonado Instituto Argentino de Investigaciones de las Zonas Áridas, CONICET y Universidad Nacional de Cuyo. Mendoza, Argentina. Programa de Posgrado en Biología (PROBIOL), Universidad Nacional de Cuyo. Mendoza, Argentina. Sección Entomología, Facultad de Ciencias, Universidad de la República. Montevideo. Uruguay
Alejandro M. Serrano Instituto Argentino de Investigaciones de las Zonas Áridas, CONICET y Universidad Nacional de Cuyo. Mendoza, Argentina. Programa de Posgrado en Biología (PROBIOL), Universidad Nacional de Cuyo. Mendoza, Argentina
Natacha P. Chacoff Instituto de Ecología Regional, CONICET-Universidad Nacional de Tucumán. Tucumán, Argentina. Facultad de Ciencias Naturales e Instituto Miguel Lillo, Universidad Nacional de Tucumán. Tucumán, Argentina
Diego P. Vazquez Instituto Argentino de Investigaciones de las Zonas Áridas, CONICET y Universidad Nacional de Cuyo. Mendoza, Argentina. Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Cuyo. Mendoza, Argentina

DOI:

https://doi.org/10.25260/EA.23.33.2.0.2075

Palabras clave:

escarabajos estercoleros, semillas, dispersión, aridez, desierto, pastoreo

Resumen

Los escarabajos estercoleros pueden influenciar la emergencia y supervivencia de plántulas. Sin embargo, la dirección y la magnitud de este efecto dependerá de los atributos funcionales de la comunidad de escarabajos estercoleros y de las condiciones ambientales dominantes. Estudiamos el rol de los escarabajos estercoleros en la dispersión de semillas de Prosopis flexuosa DC. en un ambiente árido. Realizamos un estudio experimental para evaluar la efectividad de cuatro especies de escarabajos estercoleros en la dispersión secundaria de semillas. Para ello, seleccionamos cuatro especies de escarabajos estercoleros que pertenecen a distintos grupos funcionales: levantadores, cavadores y rodadores. Los escarabajos estercoleros removieron entre 0.7%-7.5% de las semillas embebidas en el estiércol de vaca. El efecto neto de los escarabajos sobre la emergencia de plántulas y su supervivencia varía marcadamente entre especies: Malagoniella puncticollis (rodador) tuvo un efecto neutro sobre la emergencia de plántulas y positivo en la supervivencia. Sulcophanaeus imperator, Digitonthophagus gazella (cavadores) y Eucranium arachnoides (levantadores) tuvieron un efecto positivo sobre la emergencia de plántulas; sin embargo, el efecto de S. imperator sobre la supervivencia de plántulas fue negativo, y los efectos de D. gazella y E. arachnoides, neutros. Nuestros resultados indican que, aunque los escarabajos estercoleros remueven pocas semillas de P. flexuosa, su rol principal consistió en cambiar las condiciones microambientales para las semillas que permanecen en el estiércol.

Fotos: Luciana Quiroga (A), Diego N. Mirás (B and C), Belén Maldonado (D)

Citas

Andresen, E. 2002. Dung beetles in a Central Amazonian rainforest and their ecological role as secondary seed dispersers. Ecological Entomology 27: 257-270. https://doi.org/10.1046/j.1365-2311.2002.00408.x.

Andresen, E. 2003. Effect of forest fragmentation on dung beetle communities and functional consequences for plant regeneration. Ecography 26:87-97. https://doi.org/10.1034/j.1600-0587.2003.03362.x.

Andresen, E., and D. J. Levey. 2004. Effects of dung and seed size on secondary dispersal, seed predation, and seedling establishment of rainforest trees. Oecologia 139:45-54. https://doi.org/10.1007/s00442-003-1480-4.

Andresen, E., and F. Feer. 2005. The Role of Dung Beetles as Secondary Seed Dispersers and their Effect on Plant Regeneration in Tropical Rainforests. Pp. 331-349 in J. E. Lambert, P. E. Hulme and S. B. Vander Wall (eds.). Seed Fate: Predation, Dispersal, and Seedling Establishment. CABI International, Wallingford, Oxfordshire, UK. https://doi.org/10.1079/9780851998060.0331.

Ardali, E. O., P- Tahmasebi, D. Bonte, T. Milotic, I. R. Pordanjani, and M. Hoffmann. 2016. Ecological sustainability in rangelands: the contribution of dung beetles in secondary seed dispersal (case study: Chaharmahal and Bakhtiari province, Iran). European Journal of Sustainable Development 5:133-139. https://doi.org/10.14207/ejsd.2016.v5n3p133.

Aschero, V., W. F. Morris, D. P. Vázquez, J. A. Álvarez, and P. E. Villagra. 2016. Demography and population growth rate of the tree Prosopis flexuosa with contrasting grazing regimes in the Central Monte Desert. Forest Ecology and Management 369:184-190. https://doi.org/10.1016/j.foreco.2016.03.028.

Barbero, E., and Y. López-Guerrero. 1992. Some considerations on the dispersal power of Digitonthophagus gazella (Fabricius 1787) in the New World (Coleoptera Scarabaeidae Scarabaeinae). Tropical Zoology 5:115-120. https://doi.org/10.1080/03946975.1992.10539184.

Bates, D., M. Maechler, and B. Bolker. 2012. lme4: Linear mixed-effects models using S4 classes. URL: cran.r-project.org/web/packages/lme4/index.html.

Braga, R. F., R. Carvalho, E. Andresen, D. V. Anjos, E. Alves-Silva, and J. Louzada. 2017. Quantification of four different post-dispersal seed deposition patterns after dung beetle activity. Journal of Tropical Ecology 33:407-410. https://doi.org/10.1017/S0266467417000335.

Breheny, P., and W. Burchett. 2017. Visualization of Regression Models Using visreg. The R Journal 9:56-71. https://doi.org/10.32614/RJ-2017-046.

Campos, C. M., and R. A. Ojeda. 1997. Dispersal and germination of Prosopis flexuosa (Fabaceae) seeds by desert mammals in Argentina. Journal of Arid Environments 35:707-714. https://doi.org/10.1006/jare.1996.0196.

Campos, C. M., V. E. Campos, A. Mongeaud, C. E. Borghi, C. De los Ríos, and S. M. Giannoni. 2011. Relationships between Prosopis flexuosa (Fabaceae) and cattle in the Monte desert: Seeds, seedlings and saplings on cattle-use site classes. Revista Chilena de Historia Natural 84:289-299. URL: redalyc.org/articulo.oa?id=369944298013.

Campos, C. M., and S. Velez. 2015. Almacenadores y frugívoros oportunistas: el papel de los mamíferos en la dispersión del algarrobo (Prosopis flexuosa DC) en el desierto del Monte, Argentina. Revista Ecosistemas 24:28-34. https://doi.org/10.7818/ECOS.2015.24-3.05.

Chacoff, N. P., D. P. Vázquez, S. B. Lomáscolo, E. L. Stevani, J. Dorado, and B. Padrón. 2012. Evaluating sampling completeness in a desert plant-pollinator network. Journal of Animal Ecology 81:190-200. https://doi.org/10.1111/j.1365-2656.2011.01883.x.

Chapman, C. A., L. J. Chapman, K. Vulinec, A. Zanne, and M. J. Lawes. 2003. Fragmentation and Alteration of Seed Dispersal Processes: An Initial Evaluation of Dung Beetles, Seed Fate, and Seedling Diversity 1. Biotropica 35:382-393. https://doi.org/10.1111/j.1744-7429.2003.tb00592.x.

Chambers, J. C., and J. A. MacMahon. 1994. A day in the life of a seed: movements and fates of seeds and their implications for natural and managed systems. Annual Review of Ecology and Systematics 263-292. https://doi.org/10.1146/annurev.es.25.110194.001403.

Chevrolat, L. A. 1844. d' Orbigny, Dictionaire Universel d' Histoire Naturelle.

Cony, M. A., and S. O. Trione. 1996. Germination with respect to temperature of two Argentinian Prosopis species. Journal of Arid Environments 33:225-236. https://doi.org/10.1006/jare.1996.0058.

Culot, L., M. C. Huynen, and E. W. Heymann. 2018. Primates and dung beetles: two dispersers are better than one in secondary forest. International Journal of Primatology 39:397-414. https://doi.org/10.1007/s10764-018-0041-y.

Doube, B. M. 1990. A functional classification for analysis of the structure of dung beetle assemblages. Ecological Entomology 15:371-383. https://doi.org/10.1111/j.1365-2311.1990.tb00820.x.

Estrada, A., and R. Coates-Estrada. 1991. Howler monkeys (Alouatta palliata), dung beetles (Scarabaeidae) and seed dispersal: ecological interactions in the tropical rain forest of Los Tuxtlas, Mexico. Journal of Tropical Ecology 7:459-474. https://doi.org/10.1017/S026646740000585X.

Fabricius, J. C. 1781. Species insectorum exhibens eorum differentias specificas, synonyma auctorum, loca natalia, metamorphosis, adiecitis observationibus, descriptionibus. Tomus I. Carol Ernest Bohnii, Hamburg and Kiel, Germany VIII. Pp. 552. https://doi.org/10.5962/bhl.title.36509.

Feer, F. 1999. Effects of dung beetles (Scarabaeidae) on seeds dispersed by howler monkeys (Alouatta seniculus) in the French Guiana rainforest. Journal of Tropical Ecology 15:129-142. https://doi.org/10.1017/S0266467499000711.

Fenner, M. 1987. Seedlings. New Phytologist 106:35-47. https://doi.org/10.1111/j.1469-8137.1987.tb04681.x.

Ffolliott, P. F., and J. L. Thames. 1983. Recolección, manipuleo, almacenaje y pretratamiento de las semillas de Prosopis en América Latina (No. FAO 634.97365 F437r). FAO, Roma (Italia). URL: fao.org/3/Q2180S/Q2180S00.htm.

Grime, J. P. 1998. Benefits of plant diversity to ecosystems: immediate, filter and founder effects. Journal of Ecology 86:902-910. https://doi.org/10.1046/j.1365-2745.1998.00306.x.

Halffter, G., and E. G. Matthews. 1966. The Natural History of Dung Beetles of the Subfamily Scarabaeinae (Coleoptera, Scarabaeidae). Folia Entomológica Mexicana 12-14. México DF. Pp. 312.

Heymons, R., and H. von Lengerken. 1929. Biologische Untersuchumgen an Coprophagen Lamellicornien: I. Nahrungserwerb und Fortpflazungsbiologie der Gattung Scarabaeus. L. Z. Zeitchrift Morphologie und Oekologie der Tiere 14:531-613. https://doi.org/10.1007/BF00419328.

Huerta, C., M. I. Martínez, E. Montes de Oca, M. Cruz Rosales, and M. E. Favila. 2013. The role of dung beetles in the sustainability of pasture and grassland. Pp. 441-463 in A. Yañez-Arancibia and R. Dávalos-Sotelo (eds.). Ecological dimensions for sustainable socio economic development. WitPress, Boston, USA. https://doi.org/10.2495/978-1-84564-756-8/024.

Ishikawa, H. 2011. Effects of dung beetles on seedling emergence from herbaceous seeds in the dung of sika deer (Cervus nippon) in a temperate Japanese grassland ecosystem. Ecological Research 26:725-734. https://doi.org/10.1007/s11284-011-0831-6.

Johnson, S. N., G. Lopaticki, K. Barnett, S. L. Facey, J. R. Powell, and S. E. Hartley. 2016. An insect ecosystem engineer alleviates drought stress in plants without increasing plant susceptibility to an above‐ground herbivore. Functional Ecology 30:894-902. https://doi.org/10.1111/1365-2435.12582.

Koike, S., H. Morimoto, C. Kozakai, I. Arimoto, M. Soga, K. Yamazaki, and M. Koganezawa. 2012. The role of dung beetles as a secondary seed disperser after dispersal by frugivore mammals in a temperate deciduous forest. Acta Oecologica 41:74-81. https://doi.org/10.1016/j.actao.2012.04.009.

Kazuhira, Y., K. Hdeaki, K. Takuro, and A. Toshiharu. 1991. Nitrogen mineralization and microbial populations in cow dung, dung balls and underlying soil affected by paracoprid dung beetles. Soil Biology and Biochemistry 23:649-653. https://doi.org/10.1016/0038-0717(91)90078-X.

López, B. C., M. Holmgren, S. Sabaté, and C. A. Gracia. 2008. Estimating annual rainfall threshold for establishment of tree species in water-limited ecosystems using tree-ring data. Journal of Arid Environments 72:602-611. https://doi.org/10.1016/j.jaridenv.2007.10.012.

Maldonado, M. B. 2017. Funciones ecológicas de un ensamble de escarabajos estercoleros (Scarabaeidae: Scarabaeinae) en un gradiente de aridez en el desierto del Monte, Argentina. Tesis doctoral. Universidad Nacional de Cuyo, Mendoza. Argentina.

Marone, L., M. E. Horno, and R. G. D. Solar. 2000. Post‐dispersal fate of seeds in the Monte desert of Argentina: patterns of germination in successive wet and dry years. Journal of Ecology 88:940-949. https://doi.org/10.1046/j.1365-2745.2000.00508.x.

Monteresino, E. M., and M. Zunino. 2003. Sobre el comportamiento de alimentación y nidificación de Eucraniini (Coleoptera Scarabaeidae: Scarabaeinae). Pp. 75-80 in G. Onore, P. Reyes Castillo and M. Zunino (eds.). Escarabeidos de Latinoamérica: Estado del conocimiento. Sociedad Entomológica Aragonesa, SEA, España.

Morales-Alba, A., I. Morales, and F. Alvarado. 2022. Bigger and stronger bury deeper: the role of dung beetles as secondary seed dispersers in the northern Colombian Andes. International Journal of Tropical Insect Science 42:2259-2268. https://doi.org/10.1007/s42690-022-00748-z.

Nichols, E., S. Spector, J. Louzada, T. Larsen, S. Amezquita, M. E. Favila, and T. S. R. Network. 2008. Ecological functions and ecosystem services provided by Scarabaeinae dung beetles. Biological Conservation 141:1461-1474. https://doi.org/10.1016/j.biocon.2008.04.011.

Ocampo, F. C., and D. C. Hawks. 2006. Molecular phylogenetics and evolution of the food relocation behaviour of the dung beetle tribe Eucraniini (Coleoptera: Scarabaeidae: Scarabaeinae). Invertebrate Systematics 20:557-570. https://doi.org/10.1071/IS05031.

Ocampo, F. C. 2007. The Argentinean dung beetle genus Anomiopsoides (Scarabaeidae: Scarabaeinae: Eucraniini): description of a new species, and new synonymies for A. heteroclyta. Revista de la Sociedad Entomológica Argentina 66:159-168.

R Development Core Team. 2015. R: a language and environment for statistical computing. R Foundation for Statistical Computing.

Ridsdill-Smith, T. J., L. Hayles, and M. J. Palmer. 1987. Mortality of eggs and larvae of the bush fly, Musca vetustissima Walker (Diptera: Muscidae), caused by scarabaeine dung beetles (Coleoptera: Scarabaeidae) in favourable cattle dung. Bulletin of Entomological Research 77:731-736. https://doi.org/10.1017/S0007485300012220.

Shepherd, V. E., and C. A. Chapman. 1998. Dung beetles as secondary seed dispersers: impact on seed predation and germination. Journal of Tropical Ecology 14:199-215. https://doi.org/10.1017/S0266467498000169.

Urrea-Galeano, L. A., E. Andresen, R. Coates, F. M. Ardila, A. D. Rojas, and G. Ramos-Fernández. 2019. Horizontal seed dispersal by dung beetles reduced seed and seedling clumping, but did not increase short-term seedling establishment. PloS ONE 14(10):e0224366. https://doi.org/10.1371/journal.pone.0224366.

Vander Wall, S. B., and W. S. Longland. 2004. Diplochory: are two seed dispersers better than one? Trends in Ecology and Evolution 19:155-161. https://doi.org/10.1016/j.tree.2003.12.004.

Vander Wall, S. B., and W. S. Longland. 2005. Diplochory and the evolution of seed dispersal. Pp. 297-314 in J. E. Lambert, P. E. Hulme and S. B. Vander Wall (eds.). Seed Fate: Predation, Dispersal, and Seedling Establishment. CABI International Wallingford, Oxfordshire, UK. https://doi.org/10.1079/9780851998060.0297.

Velez, S., N. P. Chacoff, and C. M. Campos. 2016. Seed predation and removal from feces in a dry ecosystem. Basic and Applied Ecology 17:145-154. https://doi.org/10.1016/j.baae.2015.09.002.

Verdú, J. R., C. Numa, J. M. Lobo, M. Martínez-Azorín, and E. Galante. 2009. Interactions between rabbits and dung beetles influence the establishment of Erodium praecox. Journal of Arid Environments 73:713-718. https://doi.org/10.1016/j.jaridenv.2009.02.008.

Villagra, P. E., L. Marone, and M. A. Cony. 2002. Mechanisms affecting the fate of Prosopis flexuosa (Fabaceae, Mimosoideae) seeds during early secondary dispersal in the Monte Desert, Argentina. Austral Ecology 27:416-421. https://doi.org/10.1046/j.1442-9993.2002.01195.x.

Vulinec, K. 2002. Dung Beetle Communities and Seed Dispersal in Primary Forest and Disturbed Land in Amazonia 1. Biotropica 34:297-309. https://doi.org/10.1111/j.1744-7429.2002.tb00541.x.