Seed removal by ants in Brazilian savanna: optimizing fieldwork
Keywords:Artificial seed, ecological function, Formicidae, natural seed, sampling standardization
There has been an increase in the number of studies using seed removal by ants to evaluate ecosystem functioning; however, these studies encompassed varying time periods and used different types of seeds. Therefore, our aim was to evaluate differences in the proportion of seeds removed by ants in impacted and non-impacted sites in Brazilian savanna. Furthermore, we evaluated seed removal (1) during the morning and after a 24h period of seed exposure and (2) using natural and artificial seeds (manipulated resource to resemble natural seeds). The proportion of seeds removed was higher after the 24h exposure period (artificial seeds) regardless of site status, and more artificial seeds were removed than natural seeds. Our recommendations regarding sampling period depend on whether evaluating impacted or non-impacted sites. Although seed removal was greater after 24h in both impacted and non-impacted sites, we suggest that research evaluating the proportion of seeds removed in non-impacted sites should be performed only in the morning period to optimize the sampling time (removal of 60% during this period). When the aim is to compare non-impacted and impacted sites, we suggest evaluating after 24h of exposure, since the impacted sites experienced a higher proportion of seed removal during the afternoon and/or night time periods. Furthermore, we recommend the use of artificial seeds because they are easier to obtain and manipulate, and allow us to do comparisons between studies at different regions. We consider these findings an important first step towards standardizing future research on seed removal in Brazilian savannas by facilitating fieldwork and allowing comparisons to be made among different studies.
Adeyinka, A. M., Joseph, O. B. & Amoo, I. A. (2013). Effects of Seed Coat Absence on the Chemical Composition of Croton (Croton penduliflorus). Seed and its Oil. International Journal of Science and Research, 2: 2319-7064.
Andersen, A. N., Hertog, T. & Woinarski, J. C. Z. (2006). Long-term fire exclusion and ant community structure in an Australian tropical savanna: congruence with vegetation succession. Journal of Biogeography, 33: 823-832. doi: 10.11 11/j.1365-2699.2006.01463.x
Anjos, D., Campos, R., Campos, R. & Ribeiro, S. (2017). Monitoring Effect of Fire on Ant Assemblages in Brazilian Rupestrian Grasslands: Contrasting Effects on Ground and Arboreal Fauna. Insects, 8: 1-12. doi: 10.3390/insects8030064
Aranda-Rickert, A. & Fracchia, S. (2012). Are subordinate ants the best seed dispersers? Linking dominance hierarchies and seed dispersal ability in myrmecochory interactions. Arthropod-Plant Interactions, 6: 297-306. doi: 10.1007/s118 29-011-9166-z
Armbrecht, I. & Gallego, M. C. (2007). Testing ant predation on the coffee berry borer in shaded and sun coffee plantations in Colombian. The Netherlands Entomological Society, 124: 261-267. doi: 10.1111/j.1570-7458.2007.00574.x
Armbrecht, I. & Perfecto, I. (2003). Litter-twig dwelling ant species richness and predation potential within a forest fragment and neighboring coffee plantations of contrasting habitat quality in Mexico. Agriculture, Ecosystems and Environment, 97: 107-115. doi: 10.1016/S0167-8809(03)00128-2
Armbrecht, I., Perfecto, I. & Silverman, E. (2006). Limitation of nesting resources for ants in Colombian forests and coffee plantations. Ecological Entomology, 31: 403-410. doi: 10.11 11/j.1365-2311.2006.00802.x
Belchior, C., Del-Claro, K & Oliveira, P.S. (2012). Seasonal patterns in the foraging ecology of the harvester ant Pogonomyrmex naegelli (Formicidae, Myrmicinae) in a Naotropical savanna: daily rhytms, shifts in granivory and carnivory, and home range. Arthropod-Plant Interactions, 6: 571-582.
Bello, M. O., Abdul-Hammed, M., Adekunle, A. S. & Fasogbon, O. T. (2014). Nutrient Contents and Fatty Acids Profiles of Leaves and Seeds of Croton zambesicus. Advance Journal of Food Science and Technology, 6: 398-402.
Bieber, A. G. D., Silva, P. S. D., Sendoya, S. F. & Oliveira, P. S. (2014). Assessing the impact of deforestation of the Atlantic Rainforest on ant-fruit interactions: A field experiment using synthetic fruits. PLoS One, 9: e90369. doi: 10.1371/journal. pone.0090369
Braga, R. F., Korasaki, V., Andresen, E. & Louzada, J. (2013). Dung beetle community and functions along a habitat disturbance gradient in the Amazon: A rapid assessment of ecological functions associated to biodiversity. PLoS One, 8: e57786. doi: 10.1371/journal.pone.0057786
Christianini, A. V., Mayhé-Nunes, A. J. & Oliveira, P. S. (2007). The role of ants in the removal of non-myrmecochorous diaspores and seed germination in a neotropical savanna. Journal of Tropical Ecology, 23:343-351. doi: 10.1017/S026 6467407004087
Christianini, A. V., Mayhé-Nunes, A. J. & Oliveira, P. S. (2012). Exploitation of fallen diaspores by ants: Are there ant-plant partner choices? Biotropica, 44: 360-367. doi: 10.11 11/j.1744- 7429.2011.00822.x
Costa, B. N. S., Pinheiro, S. C. C., Amado, L. L. & Lima, M. O. (2016). Microzooplankton as a bioindicator of environmental degradation in the Amazon.Ecological Indicators, 61: 526- 545. doi: 10.1016/j.ecolind.2015.10.005
De La Mora, A., García-Ballinas, J. A. & Philpott, S. M. (2015). Local, landscape, and diversity drivers of predation services provided by ants in a coffee landscape in Chiapas, Mexico. Agriculture, Ecosystems and Environment, 201: 83- 91. doi: 10.1016/j.agee.2014.11.006
Dominguez-Haydar, Y. E. & Armbrecht, I. (2011). Response of ants and their seed removal in rehabilitation areas and forests at el Cerrejón coal mine in Colombia. Restoration Ecology, 19: 178-184.doi: 10.1111/j.1526-100X.2010.00735.x
Edwards, F. A., Edwards, D. P., Larsen, T. H., Hsu, W. W., Benedick, S., Chung, A., VunKhen, C., Wilcove, D. S. & Hamer, K. C. (2014). Does logging and forest conversion to oil palm agriculture alter functional diversity in a biodiversity hotspot? Animal Conservation, 17: 163-173. doi: 10.1111/acv.12074
Ferreira, A.V., Bruna, E.M. & Vasconcelos, H.L. (2011). Seed predators limit plant recruitment in Neotropical savanas. Oikos, 120: 1013-1022. doi: 10.1111/j.1600-0706.2010.19052.x
Folgarait, P. J. (1998). Ant biodiversity and its relationship to ecosystem functioning: a review. Biodiversity and Conservation, 7: 1221-1244.
Frouz, J. & Jilková, V. (2008). The effect of ants on soil properties and processes (Hymenoptera: Formicidae). Myrmecological News, 11: 191-199.
Gallegos, S. C., Hensen, I. & Schleuning, M. (2014). Secondary dispersal by ants promotes forest regeneration after deforestation. Journal of Ecology, 102: 659-666. doi: 10.1111/1365-2745.12226
Griffiths, H.M., Ashton, L.A., Walker, A.E., Hasan, F., Evans, T. A., Eggleton, P. & Parr C.L. (2017). Ants are the major agents of resource removal from tropical rainforests. Journal of Animal Ecology, 87: 1-9. doi: 10.1111/1365-2656.12728
Henao-Gallego, N., Escobar-Ramírez, S., Calle, Z., Montoya- Lerma, J. & Armbrecht, I. (2012). An artificial aril designed to induce seed hauling by ants for ecological rehabilitation purposes. Restoration Ecology, 20: 555-560. doi: 10.1111/j. 1526-100X.2011.00852.x
Koivula, M. T. (2011). Useful model organisms, indicators, or both? Ground beetles (Coleoptera, Carabidae) reflecting environmental conditions. ZooKeys, 100: 287-317. doi: 10.3897/ zookeys.100.1533
Leal, L. C., Andersen, A. N. & Leal, I. R. (2014). Anthropogenic disturbance reduces seed dispersal services for myrmeco-chorous plants in the Brazilian Caatinga. Oecologia, 174: 173-181. doi: 10.1007/s00442-013-2740-6
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. doi: 10.1007/s10531-012-0271-9
Lima, L.D. & Antonialli-Junior W.F. (2013) Foraging strategies of the ant Ectatomma vizottoi (Hymenoptera, Formicidae). Revista Brasileira de Entomologia, 57: 392-396. doi: 10.1590/S0085-56262013005000038
Lima, M. H. C., Oliveira, E. & Silveira, F. (2013). Interactions between ants and non-myrmecochorous fruits in Miconia (Melastomataceae) in a neotropical savanna. Biotropica, 45: 217-223. doi: 10.1111/j.1744-7429.2012.00910.x
Morris, J. R., Vandermeer, J. & Perfecto, I. (2015). A Keystone Ant Species Provides Robust Biological Control of the Coffee Berry Borer Under Varying Pest Densities. PLoS ONE, 10: e0142850. doi: 10.1371/journal.pone.0142850
Naeem, S., Chair, F. S., Chapin III, F. S., Costanza, R., Ehrlich, P. R., Golley, F. B., Hooper, D. U., Lawton, J. H., O’Neil, R. V., Mooney, H. A., Sala, O. E., Symstad, A. J. & Tilman, D. (1999). Biodiversity and ecosystem functioning: Maintaining natural life support processes. Issues in Ecology, 4: 1-11.
Paoli, A. A. S., Freitas, L. & Barbosa, J. M. (1995). Caracte-rização morfológica dos frutos, sementes e plântulas de Croton floribundus spreng. e de Croton urucurana Baill. (Euphorbiaceae). Revista Brasileira de Sementes, 17: 57-68. doi: 10.17801/0101-3122/rbs.v17n1p57-68
Parr, C. L., Andersen, A. N., Chastagnol, C. & Duffaud, C. (2007). Savanna fires increase rates and distances of seed dispersal by ants. Oecologia, 151: 33-41. doi: 10.1007/s004 42-006-0570-5
Parr, C. L., Robertson, H. G., Biggs, H. C. & Chown, S. L. (2004). Response of African savanna ants to long-term fire regimes. Journal of Applied Ecology, 41: 630-642. doi: 10.11 11/j.0021-8901.2004.00920.x
Philpott, S. M., Arendt, W. J., Armbrecht, I., Bichier, P., Diestch, T. V., Gordon, C., Greenberg, R., Perfecto, I., Reynoso-Santos, R., Soto-Pinto, L., Tejeda-Cruz, C., Williams-Linera, G., Valenzuela, O. & Zolotoff, J. M. (2008). Biodiversity loss in latin American coffee landscapes: Review of the evidence on ants, birds, and trees. Conservation Biology, 22: 1093-1105. doi: 10.1111/j.1523-1739.2008.01029.x
Philpott, S. M., Perfecto, I., Armbrecht, I. & Parr, C. L. (2010). Ant diversity and function in disturbed and changing habitats. In: Lach, L., Parr, C. & Abbott, K. L. (Eds), Ant Ecology (pp.137-156). Oxford, Oxford University.
Pirk, G.I. & Lopez-de-Casenave J. (2006). Diet and seed removal rates by the harvester ants Pogonomyrmex rastratus and Pogonomyrmex pronotalis in the central Monte desert, Argentina. Insectes Sociaux, 53: 119-125. doi: 10.1007/s000 40-005-0845-6
Pizo, M. A. & Oliveira, P. S. (2001). Size and lipid content of non-myrmechorous diaspores: Effects on the interaction with litter-foraging ants in the Atlantic rain forest of Brazil. Plant Ecology, 157: 37-52.
Rabello, A. M., Queiroz, A. C., Lasmar, C. J.,Cuissi, R. G., Canedo-Júnior, E. O.,Schmidt, F. A. & Ribas, C. R. (2015). When is the best period to sample ants in tropical areas impacted by mining and in rehabilitation process? Insectes Sociaux, 62: 227-236. doi: 10.1007/s00040-015-0398-2
Raimundo, R. L. G., Guimarães JR., P. R. G., Almeida-Neto, M. & Pizo, M. A. (2004). The Influence of Fruit Morphology and Habitat Structure on Ant-Seed Interactions: A Study with Artificial Fruits. Sociobiology, 44: 1-10.
R Development Core Team 2015. A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Ribas, C. R., Campos, R. B. F., Schmidt, F. A. &Solar, R. R. C. (2012a). Ants as Indicators in Brazil: A Review with suggestions to Improve the Use of Ants in Environmental Monitoring Programs. Psyche, 2012: 23p. doi: 10.1155/2012/636749
Ribas, C. R., Schmidt, F. A., Solar, R. R. C., Campos, R. B. F., Valentim, C. L. & Schoereder, J. H. (2012b). Ants as indicators of the success of rehabilitation efforts in deposits of gold mining tailings. Restoration Ecology, 20: 712-720. doi: 10.1111/j.1526-100X.2011.00831.x
Rocha-Ortega, M., Bartimachi, A., Neves, J., Bruna, E.M., Vasconcelos, H. L. (2017). Seed removal patterns of pioneer trees in an agricultural landscape. Plant Ecology, 218: 737- 748. doi 10.1007/s11258-017-0725-y
Santos, J. C., Delabie, J. H. C. & Fernandes, G. W. (2008). A 15-year post evaluation of the fire effects on ant community in an area of Amazonian forest. Revista Brasileira de Entomologia, 52: 82-87.
Schmidt, F. A., Ribas, C. R. & Schoereder, J. H. (2013). How predictable is the response of ant assemblages to natural forest recovery? Implications for their use as bioindicators. Ecological Indicators, 24: 158-166. doi: 10.1016/j.ecolind. 2012.05.031
Siddig, A. A. H., Ellison, A. M., Ochs, A., Villar-Leeman, C. & Lau, M. K. (2016). How do ecologists select and use indicator species to monitor ecological change? Insights from 14 years of publication in Ecological Indicators. Ecological Indicators, 60: 223-230. doi: 10.1016/j.ecolind.2015.06.036
Traniello, J. F. A. (1989). Foraging strategies of ants. Annual Reviews Entomology, 34: 191-210.
Uehara-Prado, M. (2005). Effects of land use on ant species composition and diaspore removal in exotic grasslands in the Brazilian Pantanal (Hymenoptera: Formicidae). Sociobiology, 45: 915-923.
Vasconcelos, H. L., Vilhena, J. M. S., Magnusson, W. E. & Albernaz, A. L. K. M. (2006). Long-term effects of forest fragmentation on Amazonian ant communities. Journal of Biogeography, 33: 1348-1356. doi: 10.1111/j.1365-2699.2006. 01516.x
Williams, E. R., Mulligan, D. R., Erskine, P. D. & Plowman, K. P. (2012). Using insect diversity for determining land restoration development: Examining the influence of grazing history on ant assemblages in rehabilitated pasture. Agriculture, Ecosystems and Environment, 163: 54-60. doi: 10.1016/j. agee.2012.02.017
Zelikova, T. J. & Breed, M. D. (2008). Effects of habitat disturbance on ant community composition and seed dispersal by ants in a tropical dry forest in Costa Rica. Journal of Tropical Ecology, 24: 309-316. doi: 10.1017/S0266467408004999
How to Cite
Sociobiology is a diamond open access journal which means that all content is freely available without charge to the user or his/her institution. Users are allowed to read, download, copy, distribute, print, search, or link to the full texts of the articles in this journal without asking prior permission from the publisher or the author. This is in accordance with the BOAI definition of open access.
Authors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
- Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).