Evaluation of sampling techniques and influence of environmental variables on ants in forest fragments in an oil extraction area in the Amazon
DOI:
https://doi.org/10.13102/sociobiology.v67i3.5148Keywords:
Biodiversty surveys, Formicidae, Manaus, Petroleum, Tropical forestAbstract
Around the world, urban landscapes are environments modified by man, generally related to low diversity. The efficiency of a biodiversity inventory is linked to the choice of the sampling technique since the taxonomic and ecological responses of the taxons vary between methods. Here we investigate differences in the ant’s composition sampled using three different techniques in two fragments of the urban forest in the Brazilian Amazon. We also assessed whether the different techniques maintained the same ecological responses. We sampled 12 collection points at each fragment, at vegetation, and manual collection and Winkler extractor on the ground. At the same points, soil samples were collected to determine their granulometry, pH, and concentrations of organic matter, sodium, phosphorus, and potassium. We collected 115 taxa and 4720 ants. The Cururu was the richest site with more species in general, as well as in the techniques of manual collection and Winkler. We detected a complementary effect on sampling techniques, which collected different ants’ assemblages. The potassium concentration positively influenced the assemblage’s composition, but its effect varies according to the sampling techniques used. The studied fragments revealed diversity very similar to those registered in continuous Amazonian forests. The use of sampling techniques together improves the representation of the diversity of ants in the studied fragments. Edaphic environmental variables seem to have a predominant effect on ants, affecting their distribution in the landscape even in urban fragments. This highlights the importance of urban forest fragments and their inherent ecological processes.Downloads
References
Adis, J. (1990). Thirty million arthropod species: too many or too few? Journal of Tropical Ecology, 6: 115-118.
Adis, J. (1997). Terrestrial invertebrates: survival strategies, group spectrum, dominance and activity patterns. In Junk, W.J. (Ed.), The Central Amazon Floodplain. Ecological Studies 126 (pp. 299-317). Berlin: Springer-Verlag Berlin Heidelberg.
Adis, J., Harvey, M. (2000). How many Arachnida and Miriapoda are there word-wide and in Amazônia? Studies of Neotroical Fauna & Environment, 35(2): 139-141.
Aguiar, N.O., Gualberto, T.L. & Franklin, E. (2006). Medium-spatial scale pattern distribution of Pseudoscorpionida (Arachnida) in a grandient of topography (altitude and inclination) soil factors, and litter in a central Amazon forest reserve, Amazonas, Brazil. Brazilian Journal of Biology, 66(3): 29-41. doi: 10.1590/S1519-69842006000500004
Andersen, A.N. & Majer, JD. (2004). Ants show the way down under: invertebrates as bioindicators in land management. Frontiers in Ecology and the Enviroment, 2(6):291-298. doi: 10.1890/1540-9295(2004)002[0292:ASTWDU]2.0.CO;2
Baccaro, F.B., Feitosa, R., Fernández, F., Fernandes, I., Izzo, T., Souza, J.L.P. & Solar, R. (2015). Guia para os gêneros de formigas do Brasil. Manaus: Editora INPA, 388 p. doi: 10.5281/zenodo.32912.
Bestelmeyer B.T., Agosti, D., Alonso, L.E., Brandão, C.R.F., Brown Jr, W.L., Delabie J. H. C. & Silvestre, R. (2000). Field techniques for the study of ground-dwelling ants. In D. Agosti, J. D. Majer, L. E. Alonso & T. R. Schultz (Eds.), Ants: standard methods for measuring and monitoring biodiversity (pp. 122-144). Washington: Smithsonian Institution Press.
Borcard, D., Gillet, F. & Legendre, P. (2011). Numerical Ecology With R. doi: 10.1007/978-1-4419-7976-6.
Bromham, L., Cardillo, M., Bennett, A. & Elgar, M. (1999). Effects of stock grazing on the ground invertebrate fauna of woodland remnants. Austral Ecology, 24 (3). doi: 10.1046/j.1442-9993.1999.00963.x.
Brühl, C., Eltz, T. & Linsenmair, K.E. (2003). Size does matter - Effects of tropical rainforest fragmentation on the leaf litter ant community in Sabah, Malaysia. Biodiversity and Conservation, 12: 1371-1389. doi: 10.1023/A:1023621609102
Cardoso, P., Leather, S.R. (2019). Predicting a global insect apocalypse. Insect Conservation and Diversity, 12: 263–267. doi:10.1111/icad.12367
Chao, A., Gotelli, N.J., Hsieh, T.C., Sander, E.L., Ma, K.H., Colwell, R.K. & Ellison, A.M. (2014). Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecological Monographs, 84: 45–67. doi: 10.1890/13-0133.1
Chao, A. & Jost, L. (2012). Coverage-based rarefaction and extrapolation: standardizing samples by completeness rather than size. Ecology, 93, 2533–2547. doi: 10.2307/41739612
Colwell, R.K., Chao, A., Gotelli, N.J., Lin, S.-Y., Mao, C.X., Chazdon, R.L. & Longino, J.T. (2012). Models and estimators linking individual-based and sample-based rarefaction, extrapolation and comparison of assemblages. Journal of Plant Ecology, 5: 3–21. doi: 10.1093/jpe/rtr044
Couceiro, S. R. M., Forsberg, B. R., Hamada, N. & Ferreira, R. L. M. (2006). Effects of an oil spill and discharge of domestic sewage on the insect fauna of Cururu stream Manaus, Am. Brazil. Brasilian Journal of Biology, 66 (1A): 35 – 44.
Dambros, C. S., Morais, J. W., Azevedo, R. A. & Gotelli, N. J. (2016). Isolation by distance, not rivers, control the distribution of termite species in the Amazonian rain forest. Ecography. doi: 10.1111/ecog.02663
Delabie, J.H.C., Fisher, B.L., Majer, J.D. & Wrigth, I.W. (2000). Sampling effort and choice of methods, p. 145-154. In D. Agosti, J. D. Majer, L. E. Alonso & T. R. Schultz (Eds.), Ants: standard methods for measuring and monitoring biodiversity (pp. 145-154). Washington, Smithsonian Institution Press.
Erwin, T.L. (1982). Tropical forests: Their richness in Coleoptera and other Arthropod species. The Coleopterists Bulletin, 36(1): 74-75.
Fernandes, I.O. & Souza, J.L.P. (2018). Dataset of long-term monitoring of ground-dwelling ants (Hymenoptera: Formicidae) in the influence areas of a hydroelectric power plant on the Madeira River in the Amazon Basin. Biodiversity Data Journal, 6, e24375. doi: 10.3897/BDJ.6.e24375
Fisher, B.L. (1999). Improving Inventory Efficiency: A Case Study of Leaf-Litter Ant Diversity in Madagascar. Ecological Applications, 9: 714-731. doi: 10.2307/2641157.
Fittkau, E.J. & Klinge, H. (1973). On biomass and trophic structure of the Central Amazonian rain forest ecosystem. Biotropica, 5: 2-14. doi: 10.2307/2989676
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
Fox J, W.S. (2019). An R Companion to Applied Regression, Third edition. Sage, Thousand Oaks CA. https://socialsciences.mcmaster.ca/jfox/Books/Companion/.
Garden, J.G., McAlpine, C.A., Possingham, H.P. & Jones, D.N. (2007). Using multiple survey methods to detect terrestrial reptiles and mammals: What are the most successful and cost-efficient combinations? Wildlife Research, 34 (3): 218-227. doi: 10.1071/WR06111
Gardner, T.A., Barlow, J., Araujo, I.S., Ávila‐Pires, T.C., Bonaldo, A.B., Costa, J.E., Esposito, M.C., Ferreira, L.V., Hawes, J., Hernandez, M.I.M., Hoogmoed, M.S., Leite, R.N., Lo‐Man‐Hung, N.F., Malcolm, J.R., Martins, M.B., Mestre, L.A.M., Miranda‐Santos, R., Overal, W.L., Parry, L., Peters, S.L., Ribeiro‐Junior, M.A., Da Silva, M.N.F., Da Silva Motta, C. and Peres, C.A. (2008). The cost‐effectiveness of biodiversity surveys in tropical forests. Ecology Letters, 11: 139-150. doi: 10.1111/j.1461-0248.2007.01133.x
Gomes, C.B., Souza, J.L.P. & Franklin, E. (2018). A comparison between time of exposure, number of pitfall traps and the sampling cost to capture ground-dwelling poneromorph ants (Hymenoptera: Formicidae). Sociobiology, 65: 138–148. doi: 10.13102/sociobiology.v65i2.1207
Gotelli, N.J.G., Ellison, A.M., Dunn, R.R. & Sanders, N. (2011). Counting ants (Hymenoptera: Formicidae): biodiversity sampling and statistical analysis for myrmecologists. Myrmecological News, 15: 13–19.
Hawkins, C. P., Norris, R.H., Houge, J.N. & Feminella, J.W. (2000). Development and evaluation of predictive models for measuring the biological integrity of steams. Ecology Applications, 10: 1456-1477. doi: 10.1890/1051-0761(2000)010[1456:DAEOPM]2.0.CO;2
Hölldobler, B. & Wilson, E.O. (1990). The Ants. Cambridge: Harvard University Press, 732 p
Hsieh, T.C., Ma, K.H. & Chao, A. (2016). iNEXT: An R package for interpolation and extrapolation of species diversity (Hill numbers). Methods in Ecology and Evolution, 7: 1451–1456. doi: 10.1111/2041-210X.12613
Hsieh, T.C., Ma, K.H. & Chao, A. (2019). iNEXT: iNterpolation and EXTrapolation for species diversity. R package version 2.0.19 URL: http://chao.stat.nthu.edu.tw/blog/software-download/.
Hubbell, S.P. & Foster R.B. (1992). Short-term dynamics of a neotropical forest: why ecological research matters to tropical conservation and management. Oikos. 63:48-61.
Kaspari, M., Yanoviak, S.P., Dudley, R., Yuan, M. & Clay, N.A. (2009). Sodium shortage as a constraint on the carbon cycle in an inland tropical rainforest. Proceedings of the National Academy of Sciences, 106(46): 19405-19409. doi: 10.1073/pnas.0906448106
King, J. & Porter, S.D. (2005). Evaluation of Sampling Methods and Species Richness Estimators for Ants in Upland Ecosystems in Florida. Enviromental Entomology, 34: 1566–1578. doi: 10.1603/0046-225X-34.6.1566
Lewinsohn, T.M. (2006). Avaliação do estado de conhecimento da biodiversidade brasileira – volume I / Thomas Michael Lewinsohn; organizador. Brasília: MMA. 269 p
Lopes, C.T. & Vasconcelos, H.L. (2008). Evaluation of Three Methods for Sampling Ground-Dwelling Ants in the Brazilian Cerrado. Neotropical Entomology, 37: 399–405. doi: 10.1590/S1519-566X2008000400007
López-Moreno, I.R., Diaz-Betancourt, M.E. & Landa, T.S. (2003). Insectos Sociales en Ambientes Antropizados: Las Hormigas de la Ciudad de Coatepec, Veracruz, México. Sociobiology, 42: 605-622.
Magnusson, W., Lawson, B., Baccaro, F., Castilho, C., Costa, F., Castley, J.G., Drucker, D., Franklin, E., Lima, A., Luizão, R., Mendonça, F., Pezzini, F., Schietti, J., Toledo, J., Tourinho, A.,
Verdade, L.M. & Hero, J-M. (2014). Multitaxa Surveys: Integrating Ecosystem Processes and User Demands. Applied Ecology and Human Dimensions in Biological Conservation. In L.M. Verdade, M.C. Lyra-Jorge & C.I. Piña (Eds.), Applied Ecology and Human Dimensions in Biological Conservation (177-187). Springer.
Marshall, E. & Shortle, J. (2005). Using DEA and VEA to evaluate quality of life in the mid-Atlantic States. Agricultural and Resource Economics Review, 34. doi: 10.1017/S1068280500008352
McIntyre, N.E., Rango, J., Fagan, W.F. & Faeth, S. (2001). Ground arthropod community structure in a heterogeneous urban environment. Landscape and Urban Planning, 52: 257-274. doi: 10.1016/S0169-2046(00)00122-5
McKinney, M.L. (2002). Urbanization, biodiversity, and conservation. BioScience 52: 883–890. doi: 10.1641/0006-3568(2002)052[0883:UBAC]2.0.CO;2
Menke, S.B., Guenard, B., Sexton, J.O., Weiser, M.D., Dunn, R.R. & Silverman, J. (2011). Urban areas may serve as habitat and corridors for dry-adapted, heat tolerant species; an example from ants. Urban Ecosystems, 14: 135–163. doi: 10.1007/s11252-010-0150-7
Mezger, D. & Pfeiffer, M. (2011). Partitioning the impact of abiotic factors and spatial patterns on species richness and community structure of ground ant assemblages in four Bornean rainforests. Ecography, 34: 39-48. doi: 10.1111/j.1600-0587.2010.06538.x
Moraes, J., Franklin, E., Morais, J.W. & Souza, J.L.P. (2011). Species diversity of edaphic mites (Acari: Oribatida) and effects of topography, soil properties and litter gradients on their qualitative and quantitative composition in 64 km2 of forest in Amazonia. Experimental & Applied Acarology, 55: 39-63. doi: 10.1007/s10493-011-9451-7
Moreno, C.E., Guevara, R., Sánchez-Rojas, G., Téllez, D. & Verdú, J.R. (2008). Community level patterns in diverse systems: A case study of litter fauna in a Mexican pine-oak forest using higher taxa surrogates and re-sampling methods. Acta Oecologica, 33: 73–84. doi:10.1016/j.actao.2007.09.002
National Research Council. (1992). Conserving Biodiversity: A Research Agenda for Development Agencies. National Academies Press, Washington, D.C. Retrieved from http://www.nap.edu/catalog/1925
Niemelä, J. (1999). Ecology and urban planning. Biodiversity and Conservation, 8: 119-131. doi: 10.1023/A:1008817325994
Oliveira, P.Y., Souza, J.L.P., Baccaro, F.B. & Franklin, E. (2009). Ant species distribution along a topographic gradient in a terra-firme forest in Central Amazon. Pesquisa Agropecuária Brasileira, 44(8): 852-860. doi:10.1590/S0100-204X2009000800008
Olson, D.M. (1991). A Comparison of the Efficacy of Litter Sifting and Pitfall Traps for Sampling Leaf Litter Ants (Hymenoptera, Formicidae) in a Tropical Wet Forest, Costa Rica. Biotropica, 23: 166-172. doi: 10.2307/2388302
Oksanen, J., Blanchet, F.G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., Minchin, P.R., O’Hara, R.B., Simpson, G.L., Solymos, P., Stevens, M.H.H., Szoecs, E. & Wagner, H. (2019). Vegan: community ecology package. Version 2.5-6.
Parr, C. & Chown, S. (2001). Inventory and Bioindicator Sampling: Testing Pitfall and Winkler Methods with Ants in a South African Savanna. Journal of Insect Conservation, 5: 27-36. doi: 10.1023/A:1011311418962
Pik, A., Oliver, I. & Beattie, A. (2009). Taxonomic sufficiency in ecological studies of terrestrial invertebrates. Australian Journal of Ecology, 24: 555 - 562. doi: 10.1046/j.1442-9993.1999.01003.x
R Core Team. (2019). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
Roy, D.B., Rothery, P. & Brereton, T. (2007). Reduced-effort schemes for monitoring butterfly populations. Journal of Applied Ecology, 44: 993–1000. doi: 10.1111/j.1365-2664.2007.01340.x
Ribeiro-Junior, M.A., Gardner, T.A. & Ávila-Pires, T.C.S. (2008). Evaluating the Effectiveness of Herpetofaunal Sampling Techniques across a Gradient of Habitat Change in a Tropical Forest Landscape. Journal of Herpetology, 42(4): 733-749. doi: 10.1670/07-097R3.1
Sánchez-Bayo, F., Wyckhuys, K.A.G. (2019). Worldwide decline of the entomofauna: A review of its drivers. Biological Conservation, 232: 8–27. doi:10.1016/j.biocon.2019.01.020
Santos, M.N. (2016). Research on urban ants: approaches and gaps. Insectes Sociaux, 63: 359–371. doi: 10.1007/s00040-016-0483-1
Savard, J.P., Clergeau, P. & Mennechez, G. (2000). Biodiversity concepts and urban ecosystems. Landscape and Urban Planning, 48: 131-142. doi: 10.1016/S0169-2046(00)00037-2
Scott, J.M., Csuti, B., Jacobi, J.D. & Estes, J.E. (1987). Species richness. A geographical approach to protecting future biological diversity. Bioscience, 37: 782-788.
Souza, J.L.P., Baccaro, F.B., Landeiro, V.L., Franklin, E. & Magnusson, W.E. (2012). Trade-offs between complementarity and redundancy in the use of different sampling techniques for ground-dwelling ant assemblages. Applied Soil Ecology, 56: 63–73. doi: 10.1016/j.apsoil.2012.01.004
Souza, J.L.P., Baccaro, F.B., Pequeno, P.A.C.L., Franklin, E. & Magnusson, W.E. (2018). Effectiveness of genera as a higher-taxon substitute for species in ant biodiversity analyses is not affected by sampling technique. Biodiversity and Conservation, 27: 3425–3445. doi: 10.1007/s10531-018-1607-x
Souza, J.L.P., Moura, C.A.R. & Franklin, E. (2009). Cost-efficiency and information reduction in inventories of ants in an Amazonian forest reserve. Pesquisa Agropecuária Brasileira, 44(8): 940-948. doi: 10.1590/S0100-204X2009000800021
Souza, J.L.P., Moura, C.A.R., Harada, A.Y. & Franklin, E. (2007). Diversidade de espécies dos gêneros de Crematogaster, Gnamptogenys e Pachycondyla (Hymenoptera: Formicidae) e complementaridade dos métodos de coleta durante a estação seca numa estação ecológica no estado do Pará, Brasil. Acta Amazonica, 37, 649–656. doi: 10.1590/S0044-59672007000400022
Tarli, V.D., Pequeno, P.A.C.L., Franklin, E., Morais, J.W., Souza, J.L.P., Oliveira, A.H.C. & Guilherme, D.R. (2014). Multiple Environmental Controls on Cockroach Assemblage Structure in a Tropical Rain Forest. Biotropica, 46: 598-607. doi: 10.1111/btp.12138
Taylor, R.J. & Doran, D. (2001). Use of terrestrial invertebrates as indicators of the ecological sustainability of forest management under the Montreal Process. Journal of Insect Conservation, 5: 221–231. doi: 10.1023/A:1013397410297
Torres, M.T., Souza, J.L.P. & Baccaro, F.B. (2020). Distribution of epigeic and hypogeic ants (Hymenoptera: Formicidae) in ombrophilous forests in the Brazilian Amazon. Sociobiology. In press.
Vasconcelos, H.L., Macedo, A.C.C. & Vilhena, J.M.S. (2003). Influence of Topography on the Distribution of Ground-Dwelling Ants in an Amazonian Forest. Studies on Neotropical Fauna and Environment, 38: 115–124.
Vasconcelos, H.L. & Vilhena, J.M.S. (2006). Species Turnover and Vertical Partitioning of Ant Assemblages in the Brazilian Amazon: A Comparison of Forests and Savannas. Biotropica, 38: 100–106. doi: 10.1111/j.1744-7429.2006.00113.x
Vasconcelos, H.L., Vilhena, J.M., Facure, K.G. & Albernaz, A.L. (2010). Patterns of ant species diversity and turnover across 2000 km of Amazonian floodplain forest. Journal of Biogeography, 37: 432-440. doi: 10.1111/j.1365-2699.2009.02230.x
Vitousek, P.M., Mooney, H.A., Lubchenco, J. & Melillo, J.M. (1997). Human Domination of Earth’s Ecosystems. Science, 277: 494–499. doi:10.1126/science.277.5325.494
Wagner, D.L. (2020). Insect Declines in the Anthropocene. Annual Review of Entomology, 65: 457–480. doi:10.1146/annurev-ento-011019-025151
Yamaguchi, T. (2004). Influence of urbanization on ant distribution in parks of Tokyo and Chiba City, Japan, I. Analysis of ant species richness. Entomological Research, 19: 209-216. doi: 10.1111/j.1440-1703.2003.00625.x
Yamaguchi, T. (2005). Influence of urbanization on ant distribution in parks of Tokyo and Chiba City, Japan, II. Analysis of species. Entomological Science, 8: 17-25. doi: 10.1111/j.1479-8298.2005.00096.x
Zuquim, G., Costa, F.R.C. & Prado, J. (2007). Redução de esforço amostral vs. retenção de informação em inventários de pteridófitas na Amazônia Central. Biota Neotropica, v: 217-223. doi: 10.1590/S1676-06032007000300023
Downloads
Published
How to Cite
Issue
Section
License
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).