Abstract
Biotic invasions have become major agents of human-driven global change. One of the most virulent species for trees is the Dutch elm disease (DED) (Ophiostoma novo-ulmi). However, few are the studies that investigate its indirect impact on the fauna. In a well-preserved area of Sierra Morena (Cordoba, Spain), we report the repercussion of tree cover loss due to DED on ants (Hymenoptera, Formicidae), a bioindicator group. For 10 years, before and after DED, we studied ant assemblages in different zones with a gradient of invasion. In the most affected ones, indicator species of well-preserved habitats decreased, while generalist and opportunist species increased. The forest management practices undertaken after the disease had an even more devastating effect, and thus the logging and removal of dead trees in the Bejarano stream caused that its ant assemblage became more similar to the one of a nearby meadow than to the ones of close riparian areas.
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Agosti, D., Majer, J. D., Alonso, L. E., & Schultz, T. R. (Eds.). (2000). Ants: Standard methods or measuring and monitoring biodiversity. Washington, DC: Smithsonian Institution Press.
Andersen, A. N. (1997). Using Ants as bioindicators: Multiscale issues in ant community ecology. Conservation Ecology, 1, 1–8.
Andersen, A. N. (2018). Responses of ants communities to disturbance: Five principles for understanding the disturbance dynamics of a globally dominant faunal group. Journal of Animal Ecology, 1, 1–13.
Andersen, A. N., & Majer, J. D. (2004). Ants show the way down under: Invertebrates as bioindicators in land management. Frontiers in Ecology and the Environment, 2, 291–298.
Andersen, A. N., Penman, T. D., Debas, N., & Houadria, M. (2009). Ant community responses to experimental fire and logging in a eucalypt forest of south-eastern Australia. Forest Ecology and Management, 258, 188–197.
Andrew, N., Rodgerson, L., & York, A. (2000). Frequent fuel-reduction burning: The role of logs and associated leaf litter in the conservation of ant biodiversity. Austral Ecology, 25, 99–107.
Arnan, X., Gracia, M., Comas, L., & Retana, J. (2009). Forest management conditioning ground ant community structure and composition in temperate conifer forests in the Pyrenees Mountains. Forest Ecology and Management, 258, 51–59.
Bengtsson, J., Nilsson, S. G., Franc, A., & Menozzi, P. (2000). Biodiversity, disturbaces, ecosystem function and management of European forests. Forest Ecology and Management, 132, 39–50.
Berville, L., Hefetz, A., Espadaler, X., Lenoir, A., Renucci, M., Blight, O., et al. (2013). Differentiation of the ant genus Tapinoma (Hymenoptera: Formicidae) from the Mediterranean Basin by species-specific cuticular hydrocarbon profiles. Myrmecological News, 18, 77–92.
Bey, C. F. (1990). Ulmus americana. In R. M. Burns & B. H. Honkala (Eds.), Silvics of North America (Vol. 2, pp. 801–807). Washington, DC: Hardwoods USDA Forest Service.
Blatrix, R., Lebas, C., Galkowski, C., Wegnez, P., Pimenta, R., & Morichon, D. (2016). Vegetation cover and elevation drive diversity and composition of ant communities (Hymenoptera: Formicidae) in a Mediterranean ecosystem. Myrmecological News, 22, 119–127.
Boyd, I. L., Freer-Smith, P. H., Gilligan, C. A., & Godfray, H. C. J. (2013). The consequence of tree pests and diseases for ecosystem services. Science, 342, 1235773.
Brasier, C. M. (1991). Ophiostoma novo-ulmi sp. nov., causative agent of current DED pandemics. Mycopathologia, 115, 151–161.
Castracani, C., Grasso, D. A., Fanfani, A., & Mori, A. (2010). The ant fauna of Castelporziano Presidential Reserve (Rome, Italy) as a model for the analysis of ant community structure in relation to environmental variation in Mediterranean ecosystems. Journal of Insect Conservation, 14, 585–594.
Caudullo, G., & De Rigo, D. (2016). Ulmus-elms in Europe: Distribution, habitat, usage and threats. In J. San-Miguel-Ayanz, D. De Rigo, G. Caudullo, T. Houston Durrant, & A. Mauri (Eds.), European Atlas of forest tree species (pp. 137–139). Luxembourg: Publication Office of the European Union.
Chen, X., Adams, B., Bergeron, C., Sabo, A., & Hooper-Bui, L. (2015). Ant community structure and response to disturbances on coastal dunes of Gulf of Mexico. Journal of Insect Conservation, 19, 1–13.
Coggan, N. V., & Gibb, H. (2019). Digging mammal reintroductions reduce termite biomass and alter assemblage composition along an aridity gradient. Oecologia, 191, 645–656.
Crist, T. O. (2009). Biodiversity, species interactions, and functional roles of ants (Hymenoptera: Formicidae) in fragmented landscapes: A review. Myrmecological News, 12, 3–13.
Cuautle, M., Vergara, C. H., & Badano, E. I. (2016). Comparison of ant community diversity and functional group composition associated to land use change in a seasonally dry oak forest. Neotropical Entomology, 45, 170–179.
Dekoninck, W., De Koninck, H., Baugnee, J. Y., & Maelfait, J. P. (2007). Ant biodiversity conservation in Belgian calcareous grasslands: Active management is vital. Belgian Journal of Zoology, 137, 137–146.
Ellison, A. M., Bank, M. S., Clinton, B. D., Colburn, E. A., Elliot, K., Ford, C. R., et al. (2005). Loss of foundation species: Consequences for the structure and dynamics of forested ecosystems. Frontiers in Ecology and the Environment, 3, 479–486.
Fisher, M. C., Henk, D. A., Briggs, C. J., Brownstein, J. S., Madoff, L. C., McCraw, S. L., et al. (2012). Emerging fungal threats to animal, plant and ecosystem health. Nature, 484, 186–194.
Folgarait, P. J. (1998). Ant biodiversity and its relationship to ecosystem functioning: A review. Biodiversity and Conservation, 7, 1221–1244.
Freedman, M. G., Miller, R. H., & Rogers, H. S. (2018). Landscape-level bird loss increases the prevalence of honeydew-producing insects and non-native ants. Oecologia, 188, 1263–1272. https://doi.org/10.1007/s00442-018-4273-5.
Freer-Smith, P., & Webber, J. (2017). Tree pests and diseases: The threat to biodiversity and the delivery of ecosystem services. Biodiversity and Conservation, 26, 3167–3181.
Gandhi, K. J. K., & Herms, D. A. (2010). Direct and indirect effects of alien insect herbivores on ecological processes and interactions in forests of eastern North America. Biological Invasions, 12, 389–405.
Goring, S. J., & Williams, J. W. (2017). Effect of historic land-use and climate change on tree-climate relationships in the upper Midwestern United States. Ecology Letters, 20, 461–470.
Greenslade, P. J. M., & Greenslade, P. (1977). Some effects of vegetation cover and disturbance on a tropical ant fauna. Insectes Sociaux, 24, 163–182.
Greve, M. E., Hager, J., Weisser, W. W., Schall, P., Gossner, M. M., & Feldhaar, H. (2018). Effect of forest management on temperate ant communities. Ecosphere, 9, 1–16.
Gribben, P. E., Byers, J. E., Clements, M., McKenzie, L. A., Steinberg, P. D., & Wright, J. T. (2009). Behavioural interactions between ecosystem engineers control community species richness. Ecology Letters, 12, 1127–1136.
Groc, S., Delabieb, J. H. C., Fernandez, F., Petitclerca, F., Corbarad, B., Leponcee, M., et al. (2017). Litter-dwelling ants as bioindicators to gauge the sustainability of small arboreal monocultures embedded in the Amazonian rainforest. Ecological Indicators, 82, 43–49.
Gunawardene, N. R., Majer, J. D., & Edirisinghe, J. P. (2010). Investigating residual effects of selective logging on ant species assemblages in Sinharaja Forest Reserve, Sri Lanka. Forest Ecology and Management, 259, 555–562.
Hejda, M., Hanzelka, J., Kadlec, T., Strobl, M., Pysek, P., & Reif, J. (2017). Impacts of an invasive tree across trophic levels: Species richness, community composition and resident species’ traits. Diversity and Distributions, 23, 997–1007.
Hethcoat, M. G., King, B. J., Fernandez-Castiblanco, F., Ortiz-Sepúlveda, C. M., Prada Achiardi, F. C., Edwards, F. A., et al. (2019). The impact of secondary forest regeneration on ground-dwelling ant communities in the Tropical Andes. Oecologia, 191, 475–482. https://doi.org/10.1007/s00442-019-04497-8.
Hoffmann, B. D., & Andersen, A. N. (2003). Responses of ants to disturbance in Australia, with particular reference to functional groups. Austral Ecology, 28, 444–464.
Kendrick, J. A., Ribbons, R. R., Classen, A. T., & Ellison, A. M. (2015). Changes in canopy structure and ant assemblages affect soil ecosystem variables as a foundation species declines. Ecosphere, 6, 1–21.
Kwon, T. S. (2016). What is important for ant assemblages in temperate forest soils? Journal of Asia-Pacific Biodiversity, 9, 138–143.
Kwon, T. S., Lee, C. M., & Sung, J. H. (2014). Diversity decrease of ant (Formicidae, Hymenoptera) after a forest disturbance: Different responses among functional guilds. Zoological Studies, 53, 37–47.
Leal, I. R., Filgueiras, B. K. C., Gomes, J. P., Iannuzzi, L., & Andersen, A. N. (2012). Effects of habitat fragmentation on ant richness and functional composition in Brazilian Atlantic forest. Biodiversity and Conservation, 21, 1687–1701.
Liebhold, A. M., Brockerhoff, E. G., Kalisz, S., Nuñez, M. A., Wardle, D. A., & Wingfiel, M. J. (2017). Biological invasions in forest ecosystems. Biological Invasions, 19, 3437–3458.
Lindenmayer, D. B., & Noss, R. F. (2006). Salvage logging, ecosystem processes, and biodiversity conservation. Conservation Biology, 20, 949–958.
Loo, J. A. (2009). Ecological impacts of non-indigenous invasive fungi as forest pathogens. Biological Invasions, 11, 81–96.
Lopezaraiza, M. E., Hayes, R. B., Whalley, M. R., & Memmott, J. (2007). The impact of an alien plant on a native plant-pollinator network: An experimental approach. Ecology Letters, 10, 539–550.
Lovett, G. M., Canham, C. D., Arthur, M. A., Weathers, K. C., & Fitzhugh, R. D. (2006). Forest ecosystem responses to exotic pests and pathogens in eastern North America. BioScience, 56, 395–405.
Luque, G. M., Reyes, J., & Fernández-Haeger, J. (2007). Recovery of ground ant (Hymenoptera: Formicidae) communities six years after a major environmental disaster. Environmental Entomology, 36, 337–347.
Maeto, K., & Sato, S. (2004). Impacts of forestry on ant species richness and composition in warm-temperate forests of Japan. Forest Ecology and Management, 187, 213–223.
Mahon, M. B., Campell, K. U., & Crist, T. O. (2019). Experimental effects of white-tailed deer and an invasive shrub on forest ant communities. Oecologia, 3, 633–644. https://doi.org/10.1007/s00442-019-04516-8.
Majer, J. D., Heterick, B., Gohr, T., Hughes, E., Mounsher, L., & Grigg, A. (2013). Is thirty-seven years sufficient for full return of the ant biota following restoration? Ecological Processes, 2, 19. https://doi.org/10.1186/2192-1709-2-19.
Matutano, J., Rodríguez, A., Jiménez, A., Acedo, O., & DelMoral, L. (2017). Informe Andarríos 2017. Viceconsejería de Medio Ambiente y Ordenación del Territorio. Sevilla: Junta de Andalucía.
McCary, M. A., Mores, R., Farfan, M. A., & Wise, D. H. (2016). Invasive plants have different effects on trophic structure of green and brown food webs in terrestrial ecosystems: A meta-analysis. Ecology Letters, 19, 328–335.
Miranda, P. N., Baccaro, F. B., Morato, E. F., Oliveira, M. A., & Delabie, J. H. C. (2017). Limited effects of low-intensity forest management on ant assemblages in Southwestern Amazonian forests. Biodiversity and Conservation, 26, 2435–2451.
Montoya, J. M., Woodward, G., Emmerson, M. C., & Sole, R. V. (2009). Press perturbations and indirect effects in real food webs. Ecology, 90, 2426–2433.
Mooney, H. A., & Cleland, E. E. (2001). The evolutionary impact of invasive species. PNAS, 98, 5446–5451.
Ordoñez, C., Reyes, J., & Carpintero, S. (2007). Estudio faunístico de los formícidos (Hymenoptera: Formicidae) asociados a los bosques de ribera en la provincia de Córdoba. Primeras aportaciones. Boletín SEA, 40, 367–375.
Ortiz, F. J., & Tinaut, J. A. (1988). Formícidos del litoral granadino. Orsis, 3, 145–163.
Osborne, P. (1982). Some effects of Dutch elm disease on nesting farmland birds. Bird Study, 29, 2–16.
Osborne, P. (1983). The influence of Dutch elm disease on bird population trends. Bird Study, 30, 27–38.
Osborne, P. (1985). Some effects of Dutch elm disease on the birds of a Dorset dairy farm. Journal of Applied Ecology, 22, 681–691.
Ottonetti, L., Tucci, L., & Santini, G. (2006). Recolonization patterns of ants in a rehabilitated lignite mine in Central Italy: Potential for the use of Mediterranean ants as indicators of restoration processes. Restoration Ecology, 14, 60–66.
Paap, T., Burgess, T. I., & Wingfield, M. J. (2017). Urban trees: Bridge-heads for forest pest invasions and sentinels for early detection. Biological Invasions, 19, 3515–3526.
Pacheco, R., & Vasconcelos, H. L. (2012). Habitat diversity enhances ant diversity in a naturally heterogeneous Brazilian landscape. Biodiversity and Conservation, 21, 797–809.
Palladini, J. D., Jones, M. G., Sanders, N. J., & Jules, E. S. (2007). The recovery of ant communities in regenerating temperate conifer forests. Forest Ecology and Management, 242, 619–624.
Postle, A. C., Majer, J. D., & Bell, D. T. (1986). Soil and litterinvertebrates and litter decomposition in Jarrah (Eucalyptus marginata) forest affected by Jarrah dieback fungus (Phytophthora cinnamomi). Pedobiologia, 29, 47–69.
Punttila, P., Haila, Y., Pajunen, T., & Tukia, H. (1991). Colonisation of clearcut forests by ants in the southern Finnish taiga: A quantitative survey. Oikos, 61, 250–262.
Rasool, K. G., Husain, M., Salman, S., Tufail, M., Sukirno, S., & Aldawood, A. S. (2019). DNA barcoding of the fire ant genus Solenopsis Westwood (Hymenoptera: Formicidae) from the Riyadh region, the Kingdom of Saudi Arabia. Saudi Journal of Biological Sciences. https://doi.org/10.1016/j.sjbs.2019.06.018.
Retana, J., & Cerdá, X. (2000). Patterns of diversity and composition of Mediterranean ground ant communities tracking spatial and temporal variability in the thermal environment. Oecologia, 123, 436–444.
Reyes-López, J. L., & Carpintero, S. (2013). Descripción de Temnothorax bejaraniensis nov. sp. (Hymenoptera, Formicidae), una nueva especie para la península Ibérica. Boletín SEA, 52, 23–28.
Reyes-López, J. L., & Carpintero, S. (2014). Comparison of the exotic and native ant communities (Hymenoptera: Formicidae) in urban green areas at inland, coastal and insular sites in Spain. European Journal of Entomology, 111, 421–428.
Reyes-López, J., Ruiz, N., & Fernández-Haeger, J. (2003). Community structure of ground ants: The role of single trees in a Mediterranean pastureland. Acta Oecologica, 24, 195–202.
Ribas CR, Campos RBF, Schimidt FA, Solar RRC (2012) Ants as indicators in Brazil: a review with suggestions to improve the use of ants in environmental monitoring programs. Psyche ID 636749. https://doi.org/10.1155/2012/636749.
Rich, P. M., Wood, J., Vieglais, D. A., Burek, K., & Webb, N. (1999). Guide to HemiView: Software for analysis of hemispherical photography. Cambridge: Delta-T Devices Ltd.
Roig, X., & Espadaler, X. (2010). Propuesta de grupos funcionales de hormigas para la Península Ibérica y Baleares, y su uso como bioindicadores. Iberomyrmex, 2, 28–29.
Rudgers, J. A., & Clay, K. (2008). An invasive plant-fungal mutualism reduces arthropod diversity. Ecology Letters, 11, 831–840.
Sackett, T. E., Record, S., Bewick, S., Baiser, B., Sanders, N. J., & Ellison, A. M. (2011). Response of macroarthropod assemblages to the loss of hemlock (Tsuga canadenis), a foundation species. Ecosphere, 2, 1–16.
Seifert, B., D’Eustacchio, D., Kaufmann, B., Centorame, M., Lorite, P., & Modica, M. V. (2017). Four species within the supercolonial ants of the Tapinoma nigerrimum complex revealed by integrative taxonomy (Hymenoptera: Formicidae). Myrmecological News, 24, 123–144.
Sharaf, M. R., & Aldawood, A. S. (2012). Ants of the genus Solenopsis Westwood 1840 (Hymenoptera: Formicidae) in the Arabian Peninsula with description of a new species, Solenopsis elhawagryi. PLoS ONE, 7, 1–21. https://doi.org/10.1371/journal.pone.0049485.
Smith, K. F., Behrens, M. D., & Sax, D. F. (2009). Local scale effects of disease on biodiversity. EcoHealth, 6, 287–295.
Solla, A., Burón, M., Iglesias, S., & Gil, L. (2000). Spanish program for the conservation and breeding of elms against DED. In C. P. Dunn (Ed.), The elms (pp. 295–303). Boston: Springer.
Strauss, S. Y. (1991). Indirect effects in community ecology: Their definition, study and importance. Trends in Ecology & Evolution, 6, 206–210.
Suarez, A. V., Bolger, D. T., & Case, T. J. (1998). Effects of fragmentation and invasion on native ant communities in coastal Southern California. Ecology, 79, 2041–2056.
Trussell, G. C., Ewanchuk, P. J., & Matassa, C. M. (2006). Habitat effects on the relative importance of trait-and density-mediated indirect interactions. Ecology Letters, 9, 1245–1252.
Tylianakis, J. M., Didham, R. K., Bascompte, J., & Wardle, D. A. (2008). Global change and species interactions in terrestrial ecosystems. Ecology Letters, 11, 1351–1363.
Tylor, L. J., Parker, K. G., & Pope, S. (1940). Relation of wounds to infection of American Elm by Ceratostomella ulmi, and the occurrence of spores in rainwater. Phytopathology, 30, 39–41.
Underwood, E. C., & Fisher, B. L. (2006). The role of ants in conservation monitoring: If, when, and how. Biological Conservation, 132, 166–182.
Vasconcelos, H. L. (1999). Effects of forest disturbance on the structure of ground-foraging ant communities in central Amazonia. Biodiversity and Conservation, 8, 409–420.
Vasconcelos, H. L., Vilhena, J. M. S., & Caliri, G. J. A. (2000). Responses of ants to selective logging of a central Amazonian forest. Journal of Applied Ecology, 37, 508–514.
Véle, A., Holuša, J., & Horák, J. (2016). Ant abundance increases with clearing size. Journal of Forest Research, 21, 110–114.
Welch, J. N., Fordyce, J. A., & Simberloff, D. S. (2016). Indirect impacts of invaders: A case study of the Pacific sheath-tailed bat (Emballonura semicaudata rotensis). Biological Conservation, 201, 146–151.
White, E. M., Wilson, J. C., & Clarke, A. R. (2006). Biotic indirect effects: a neglected concept in invasion biology. Diversity and Distributions, 12, 443–455.
Wills, B. D., & Landis, D. A. (2018). The role of ants in north temperate grasslands: A review. Oecologia, 186, 323–338. https://doi.org/10.1007/s00442-017-4007-0.
Wilson, J. D. (2017). Indirect effects of invasive Burmese pythons on ecosystems in Southern Florida. Journal of Applied Ecology, 54, 1251–1258.
Wootton, J. T. (2002). Indirect effects in complex ecosystems: Recent progress and future challenges. Journal of Sea Research, 48, 157–172.
Acknowledgements
We are grateful to Francisco Jiménez, Gema Trigos, Javier López, Carmen Ordoñez and Ana Moreno for field assistance. This study was partly funded by the Spanish Ministry of Science, Innovation and Universities (Project CGL2004-00674) and European FEDER funds (Compensatory Measures for the construction of the reservoir of La Brena II dam).
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Carpintero, S., Reyes-López, J. Indirect effect of the invasive exotic fungus Ophiostoma novo-ulmi (Dutch elm disease) on ants. COMMUNITY ECOLOGY 21, 133–143 (2020). https://doi.org/10.1007/s42974-020-00023-6
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DOI: https://doi.org/10.1007/s42974-020-00023-6