Wood Ant (Formica polyctena) Services and Disservices in a Danish Apple Plantation

Joachim Offenberg, Jesper Stern Nielsen, Christian Damgaard

Abstract


Ants possess properties that can be used to optimize plant production in agricultural systems. Ant services can be herbivore and pathogen protection and fertilization of their plant partners. They may, however, also harm plants by facilitating ant-attended herbivorous homopterans. To assess whether wood ants can be used in IPM-systems to improve apple production, we transplanted wood ants into a Danish apple plantation and tested whether ants (i) reduced the number of herbivores, (ii) led to higher amounts of leaf nutrients, (iii) controlled apple pathogens, (iv) increased homopteran abundance and (iv) whether these effects affected apple yields. During a two year study, we found that the wood ants significantly reduced the numbers of winter moth larvae, increased magnesium content in apple leaves (but did not affect 10 other nutrients), reduced the number of apples infected with apple brown rot and apple scab (on one apple variety) and increased aphid infections. In the first year, this led to higher apple production on ant trees, whereas ants had no effect on yields in the second year. It was evident that ants provided both services and disservices. If mutualistic ant-homopteran interactions can be disrupted, this would favor plant growth and open for the use of wood ants in sustainable plant management. We discuss how this may be accomplished. Alternatively, ants may be used short term to knock down pest outbreaks (before building up homopteran populations) or used in crops that do not host ant-attended homopterans.


Keywords


Integrated pest management, winter moth, plant pathogens, fertilization, ant-aphid mutualism, apple diseases.

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References


Attygalle, A.B., Siegel, B., Vostrowsky, O., Bestmann, H.J. & Maschwitz, U. (1989). Chemical composition and function of metapleural gland secretion of the ant, Crematogaster deformis Smith (Hymenoptera: Myrmicinae). Journal of Chemical Ecology, 15: 317-328. doi: 10.1007/bf02027793.

Bestmann, H.J., Kern, F., Schäfer, D. & Witschel, M.C. (1992). 3,4-Dihydroisocoumarins, a New Class of Ant Trail Pheromones. Angewandte Chemie International Edition in English, 31: 795-796. doi: 10.1002/anie.199207951.

Cushman, J.H. & Addicott, J.F. (1989). Intra- and interspecific competition for mutualists: ants as a limited and limiting resource for aphids. Oecologia, 79: 315-321. doi: 10.1007/bf00384310.

Delabie, J.H.C. (2001). Trophobiosis Between Formicidae and Hemiptera (Sternorrhyncha and Auchenorrhyncha): an Overview. Neotropical Entomology, 30: 501-516. doi: 10.1590/S1519-566X2001000400001

Folgarait, P.J. (1998). Ant biodiversity and its relationship to ecosystem functioning: A review. Biodiversity and Conservation, 7: 1221-1244. doi: 10.1023/A:1008891901953.

Frouz, J., Rybníček, M., Cudlín, P. & Chmelíková, E. (2008). Influence of the wood ant, Formica polyctena, on soil nutrient and the spruce tree growth. Journal of Applied Entomology, 132, 281-284. doi: 10.1111/j.1439-0418.2008.01285.x.

Gartnerirådgivningen (2016). Håndbog for frugt- og bæravlere. Gartnerirådgivningen, Odense, Denmark.

Gonzalez-Teuber, M., Kaltenpoth, M. & Boland, W. (2014). Mutualistic ants as an indirect defence against leaf pathogens. New Phytologist, 202, 640-650. doi: 10.1111/nph.12664.

Letourneau, D.K. (1998). Ants, stem-borers, and fungal pathogens: Experimental tests of a fitness advantage in Piper ant-plants. Ecology, 79, 593-603.

Madsen, N.E.L., Sorensen, P.B. & Offenberg, J. (2017). Sugar and amino acid preference in the black garden ant Lasius niger (L.). Journal of Insect Physiology, 100: 140-145. doi: 10.1016/j.jinsphys.2017.05.011.

Morgan, E.D. (2008). Chemical sorcery for sociality: exocrine secretions of ants (Hymenoptera: Formicidae). Myrmecological News, 11: 79-90.

Nagy, C., Cross, J.V. & Markó, V. (2013). Sugar feeding of the common black ant, Lasius niger (L.), as a possible indirect method for reducing aphid populations on apple by disturbing ant-aphid mutualism. Biological Control, 65: 24-36. doi: 10.1016/j.biocontrol.2013.01.005.

Nagy, C., Cross, J.V. & Markó, V. (2015). Can artificial nectaries outcompete aphids in ant-aphid mutualism? Applying artificial sugar sources for ants to support better biological control of rosy apple aphid, Dysaphis plantaginea Passerini in apple orchards. Crop Protection, 77: 127-138. doi: 10.1016/j.cropro.2015.07.015.

Nielsen, J.S., Nielsen, M.G., Damgaard, C. & Offenberg, J. (2018). Experiences in transplanting wood ants into plantations for integrated pest management Sociobiology, 65: 403-414. doi: 10.13102/sociobiology.v65i3.2872.

Offenberg, J. (2001). Balancing between mutualism and exploitation: the symbiotic interaction between Lasius ants and aphids. Behavioral Ecology and Sociobiology, 49, 304-310. doi: 10.1007/s002650000303.

Offenberg, J. (2014). Pest repelling properties of ant pheromones. IOBC-WPRS Bulletin, 99, 173-176.

Offenberg, J. (2015). Ants as tools in sustainable agriculture. Journal of Applied Ecology, 52, 1197-1205. doi: 10.1111/ 1365-2664.12496.

Peng, R.K. & Christian, K. (2005). Integrated pest management in mango orchards in the Northern Territory Australia, using the weaver ant, Oecophylla smaragdina, (Hymenoptera : Formicidae) as a key element. International Journal of Pest Management, 51: 149-155. doi: 10.1080/09670870500131749.

Pinkalski, C., Jensen, K.-M.V., Damgaard, C. & Offenberg, J. (2018). Foliar uptake of nitrogen from ant faecal droplets: An overlooked service to ant-plants. Journal of Ecology, 106: 289-295. doi: 10.1111/1365-2745.12841.

Rico-Gray, V. & Oliveira, P.S. (2007). The Ecology and Evolution of Ant-Plant Interactions. The University of Chicago Press, USA.

Roux, O., Céréghino, R., Solano, P.J. & Dejean, A. (2011). Caterpillars and Fungal Pathogens: Two Co-Occurring Parasites of an Ant-Plant Mutualism. PLoS ONE, 6: e20538. doi: 10.1371/journal.pone.0020538.

Rue, H., Martino, S. & Chopin, N. (2009). Approximate Bayesian inference for latent Gaussian models by using integrated nested Laplace approximations. Journal of the Royal Statistical Society: Series B (Statistical Methodology), 71: 319-392. doi: 10.1111/j.1467-9868.2008.00700.x.

Sauerländer, S. (1961). Das Gift von Formica polyctena FÖRST. als ein möglicher Schutzmechanismus dieses Insekts gegen Mikroorganismen. Die Naturwissenshaften, 48: 629.

Skinner, G.J. & Whittaker, J.B. (1981). An experimental investigation of interrelationships between the wood ant (Formica rufa) and some treew canopy herbivores. Journal of Animal Ecology, 50: 313-326. doi: 10.2307/4047.

Tena, A., Hoddle, C.D. & Hoddle, M.S. (2013). Competition between honeydew producers in an ant-hemipteran interaction may enhance biological control of an invasive pest. Bulletin of Entomological Research, 103: 714-723. doi: 10.1017/S000748531300045X.

Thornham, D., G., Smith, J., M., Ulmar, G., T. & Federle, W. (2011). Setting the trap: cleaning behaviour of Camponotus schmitzi ants increases long-term capture efficiency of their pitcher plant host, Nepenthes bicalcarata. Functional Ecology, 26, 11-19. doi: 10.1111/j.1365-2435.2011.01937.x.

Tranter, C. & Hughes, W.O.H. (2015). Acid, silk and grooming: alternative strategies in social immunity in ants? Behavioral Ecology and Sociobiology, 69, 1687-1699. doi: 10.1007/s00265-015-1980-3.

Vidkjær, N.H., Wollenweber, B., Jensen, K.M.V., Ambus, P.L., Offenberg, J. & Fomsgaard, I.S. (2016). Urea in Weaver Ant Feces: Quantification and Investigation of the Uptake and Translocation of Urea in Coffea arabica. Journal of Plant Growth Regulation, 35, 803-814. doi: 10.1007/s00344-016-9586-1.

Volkl, W., Woodring, J., Fischer, M., Lorenz, M.W. & Hoffmann, K.H. (1999). Ant-aphid mutualisms: the impact of honeydew production and honeydew sugar composition on ant preferences. Oecologia, 118, 483-491.

Wagner, D. & Fleur Nicklen, E. (2010). Ant nest location, soil nutrients and nutrient uptake by ant-associated plants: Does extrafloral nectar attract ant nests and thereby enhance plant nutrition? Journal of Ecology, 98: 614-624. doi: 10.11 11/j.1365-2745.2010.01640.x.

Way, M.J. (1954). Studies on the association of the ant Oecophylla longinoda (Latr) (Formicidae) with the scale insect Saissetia zanzibarensis Williams (Coccidae). Bulletin of Entomological Research, 45: 113-134.

Way, M.J. & Khoo, K.C. (1992). Role of ants in pest-management. Annu Rev Entomol, 37: 479-503.

Wäckers, F.L., Alberola, J.S., Garcia-Mari, F. & Pekas, A. (2017). Attract and distract: Manipulation of a food-mediated protective mutualism enhances natural pest control. Agriculture, Ecosystems and Environment, 246: 168-174. doi: 10.1016/j.agee.2017.05.037.

Zhang, Y. (2017). The antimicrobial activities of Oecophylla smaragdina. Master degree Master Thesis, Aarhus University.




DOI: http://dx.doi.org/10.13102/sociobiology.v66i2.4251

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