A New Extrafloral Nectary-Bearing Plant Species in the Brazilian Savanna and its Associated Ant Community: Nectary Structure, Nectar Production and Ecological Interactions
DOI:
https://doi.org/10.13102/sociobiology.v64i3.1603Keywords:
ants, mutualism, extrafloral nectariesAbstract
Brazilian Savanna stands out for the large number of species with extrafloral nectaries (EFNs) with high morphological diversity. In Smilax polyantha (Smilacaceae), the base of the petiole showed a slight secretion and great visitation by ants suggesting the presence of an EFN. In this way, we aimed to determine the ant community associated with this plant, as well as to identify and characterize this unsuspected structure and determine the phenology and liquid production of this tissue. The study was carried out in a Cerrado area, in Uberlândia, Brazil. Ten individuals were used for the anatomical analysis and histochemical tests and the EFNs secretory activity was monitored, being categorized into active and non-active EFN. In addition, the volume and sucrose concentration were determined from three nectaries of ten individuals, and individuals of ants found foraging on these nectary were collected, day and night. Results showed a large amount of extrafloral nectar secretion and the EFN tissue is composed of a few cell layers that showed positive reactions for proteins and reducing sugars. We recorded a significantly correlation between percentage of EFNs activity and abundance of ants. The secretory activity is concentrated in September and ten ant species, of five subfamilies, were identified foraging on the EFNs.
Downloads
References
Aguirre, A., Coates, R., Cumplido-Barragán, G., Campos-Villanueva, A. & Díaz-Castelazo, C. (2013). Morphological characterization of extrafloral nectaries and associated ants in tropical vegetation of Los Tuxtlas, Mexico. Flora, 208:147-156.doi: 10.1016/j.flora.2013.02.008
Albersheim, P., Darvill, A., Roberts, K., Sederoff, R. & Staehelin, A. (2010). Plant cell walls. Garland Science, New York. doi: 10.1093/aob/mcr128
Andreata, R.H.P. (1997). Revisão das espécies brasileiras do gênero Smilax L. (Smilacaceae). Pesquisa Botânica, 47: 7-244
Andreata, R.H.P.(2009). A new species of Smilax and a key to all species of Minas Gerais, Brazil. Systematic Botany, 34: 28-31. doi: http://dx.doi.org/10.1600/036364409787602302
Andreata, R.H.P. (2015). Smilacaceae in Lista de Espécies da Flora do Brasil. Jardim Botânico do Rio de Janeiro. http://reflora.jbrj.gov.br/jabot/floradobrasil/FB21130. (acessed date: 27 April, 2015).
Baker, J.R. (1958). Note on the use of bromophenol blue for the histochemical recognition of protein. Quarterly Journal of Microscopical Science, 99: 459-460.
Baker, H.G. & Baker, I.(1983). A brief historical review of the chemistry of floral nectar. In B. Bentley & T. Elias (Eds.),The biology of nectaries (pp 126-152). New York: Columbia University Press.
Bixenmann, R.J., Coley, P.D. & Kursar, T.A. (2011). Is extrafloral nectar production induced by herbivores or ants in a tropical facultative ant-plant mutualism? Oecologia, 165: 417-425. doi:10.1007/s00442-010-1787-x
Blüthgen, N. & Reifenrath, K. (2003). Extrafloral nectaries in an Australian rainforest: structure and distribution. Australian Journal of Botany, 51: 515-527.doi: 10.1071/BT02108
Blüthgen, N., Gottsberger, G. & Fiedler, K. (2004). Sugar and amino acid composition of ant-attended nectar and honeydew sources from an Australian rainforest. Austral Ecology, 29: 418-429.doi: 10.1111/j.1442-9993.2004.01380.x
Brundrett, M.C., Kendrick, B. & Peterson, C.A. (1991). Efficient lipid staining in plant material with Sudan Red 7B or Fluoral Yellow 088 in Polyethylene Glycol-Glycerol. Biotechnic and Histochemistry, 66: 111-116.
Bukatsch, F. (1972). Bemerkungenzur Doppelfärbung: Astrablau-Safranin. Mikrokosmos, 61: 255.
Byk, J. & Del-Claro, K. (2011). Ant-plant interaction in the Neotropical savanna: direct beneficial effects of extrafloral nectar on ant colony fitness. Population Ecology, 53: 327-332.doi:10.1007/s10144-010-0240-7
Coutinho, I.A.C., Francino, D.M.T., Azevedo, A.A. & Meira, R.M.S.A. (2012). Anatomy of the extrafloral nectaries in species of Chamaecrista section Absus subsection Baseophyllum (Leguminosae, Caesalpinioideae). Flora, 207: 427-435. doi: 10.1016/j.flora.2012.03.007
Dafni, A., Kevan, P.G. & Husband, B.C. (2005). Practical Pollination Biology. Cambridge.
Del-Claro, K., Rico-Gray, V., Torezan-Silingardi, H.M., Alves-Silva, E., Fagundes, R., Lange, D., Dáttilo, W., Vilela, A.A., Aguirre, A. & Rodriguez-Morales, D. (2016). Loss and gains in ant–plant interactions mediated by extrafloral nectar: Fidelity, cheats, and lies. Insectes Sociaux, 63: 207-221. doi: 10.1007/s00040-016-0466-2
Del-Claro, K. & Marquis, R.J. (2015). Ant species identity has a greater effect than fire on the outcome of an ant protection system in Brazilian Cerrado. Biotropica, 47 : 459-467. doi: 10.1111/btp.1222
Del-Claro, K., Guillermo-Ferreira, R., Almeida, E.M., Zardini, H. & Torezan-Silingardi, H.M. (2013). Ants visiting the post-floral secretions of pericarpialnectariesin Palicourearigida (Rubiaceae) provide protection against leaf herbivores but not against seed parasites. Sociobiology, 60: 217-221. doi: 10.13102/sociobiology.v60i3.217-221
Díaz-Castelazo, C., Rico-Gray, V., Ortega, F. & Angeles, G. (2005). Morphological and secretory characterization of extrafloral nectaries in plants of coastal Veracruz, Mexico. Annals of Botany, 96: 1175-1189.doi: 10.1093/aob/mci270
Durkee, T. (1982). The floral and extra-floral nectaries of Passiflora. II. The extra-floral nectary. American Journal of Botany, 69: 1420-1428.
Elias, T.S. (1983). Extrafloral nectaries: their structure and distribution.InB. Bentley & T.S. Elias (Eds.), The Biology of Nectaries (pp 174-203). New York: Columbia University Press.
Escalante-Pérez, M. & Heil, M. (2012). Nectar secretion: its ecological context and physiological regulation, InJ. Vivanco & F. Baluska (Eds.), Secretions and Exudates in Biological Systems Berlin (pp187-220). Springer.
Fahn, A. (1979). Secretory tissues in plants. Academic Press: London, UK.
Fahn, A. (1988). Secretory tissues in vascular plants. New Phytologist, 108: 229-257.
Fahn, A. (2000). Structure and function of secretory cells. InD. L. Hallahan, J.C. Gray & J.A. Callow (Eds.), Advances in botanical research (pp 31: 37-75). London: Academic Press.
Ferreira, C.A. & Torezan-Silingardi, H.M. (2013). Implications of the floral herbivory on Malpighiacea plant fitness: visual aspect of the flower affects the attractiveness to pollinators. Sociobiology, 60: 323-328. doi: 10.13102/sociobiology.v60i3.323-328
Gaffal, K.P. (2012). How common is the ability of extrafloral nectaries to produce nectar droplets, to secrete nectar during the night and to store starch? Plant Biology, 14: 691-695. doi: 10.1111/j.1438-8677.2012.00616.x
Galetto, L., Bernardello, G. & Rivera, G.L. (1997). Nectar, nectaries, flower visitors, andbreeding system in five terrestrial Orchidaceae from central Argentina. Journal of Plant Research, 110: 393-403.
González-Teuber, M. & Heil, M. (2009). Nectar chemistry is tailored for both attraction of mutualists and protection from exploiters. Plant Signaling and Behavior, 4: 809-813.
Heil, M. (2015). Extrafloral nectar at the plant-insect interface: a spotlight on chemical ecology, phenotypic plasticity, and food webs. Annual Reviews of Entomology, 60: 213-232. doi: 10.1146/annurev-ento-010814-020753
Heil, M. & McKey, D. (2003). Protective ant–plant interactions as model systems in ecological and evolutionary research. Annual Review of Ecology, Evolution and Systematics, 34: 425-453. doi: 10.1146/annurev.ecolsys.34.011802.132410
Heldt, H.W. & Piechulla, B. (2011). Plant Biochemistry. San Diego, Academic Press. doi: 10.1016/B978-0-12-384986-1.00022-3
Jensen, W.A. (1962). Botanical histochemistry: principles and practice. San Francisco: W.H. Freeman.
Johansen, D.A. (1940). Plant microtechnique. New York: Mc Graw-Hill Book.
Koptur, S. (1992). Plants with extrafloral nectaries and ants in everglades habitats. The Florida Entomologist, 75: 38-50.
Koptur, S. (1994). Floral and extrafloral nectars of neotropical Inga trees: a comparison of their constituents and composition. Biotropica, 26: 276-284.
Koptur, S., Rico-Gray, V. & Palacios-Rios, M. (1998). Ant protection of the nectaried fern Polypodium plebeium in Central Mexico. American Journal of Botany, 85: 736-739.
Kraus, J.E. & Arduin M. (1997). Manual básico de métodos em morfologia vegetal. Rio de Janeiro: EDUR.
Lange, D., Calixto, E.S. & Del-Claro, K. (2017). Variation in extrafloral nectary productivityinfluences the ant foraging. PLoS ONE 12(1): e0169492. doi: 10.1371/journal.pone.0169492
Lange, D., Dáttilo, W. & Del-Claro, K. (2013). Influence of extrafloral nectary phenology on ant-plant mutualistic networks in a neotropical savanna. Ecological Entomology, 38: 463-469. doi: 10.1111/een.12036
Lange, D. & Del-Claro, K. (2014). Ant-plant interaction in a tropical savanna: may the network structure vary over time and influence on the outcomes of associations? PLOS ONE 9(8): e105574. doi: 10.1371/journal.pone.0105574
Leitão, C.A.E., Dolder, M.A.H. & Cortelazzo, A.L. (2014). Anatomy and histochemistry of the nectaries of Rodriguezia venusta (Lindl.) Rchb. f. (Orchidaceae). Flora, 209: 233-243. doi: 10.1016/j.flora.2014.03.002
Liu, J.X. & Chen, J. (2008). Preliminary investigation of extrafloral nectaries plants in the tropical rainforests in Xishuangbanna, China. Acta Botanica Yunnanica, 30: 173-182. doi: 10.3724/SP.J.1143.2008.00173
Machado, S.R., Morellato, L.P.C., Sajo, M.G. & Oliveira, P.S. (2008). Morphological patterns of extrafloral nectaries in woody plant species of the Brazilian Cerrado. Plant Biology 10: 660-673. doi: 10.1111/j.1438-8677.2008.00068.x
Marazzi, B., Bronstein, J.L. & Koptur, S. (2013). The diversity: ecology and evolution of extrafloral nectaries: current perspectives and future challenges. Annals of Botany, 111: 1243-1250. doi: 10.1093/aob/mct109.
Melo, Y., Machado, S.R. & Alves, M. (2010). Anatomy of extrafloral nectaries in Fabaceae from dry-seasonal forest in Brazil. Botanical Journal of Linnean Society, 163: 87-98. doi: 10.1111/j.1095-8339.2010.01047.x
Muntz, K., Belozersky, M.A., Dunaevsky, Y.E., Schlereth, A. & Tiedemann, J. (2001). Stored proteinases and the initiation of storage protein mobilization in seeds during germination and seedling growth. Journal Experimental Botany, 52: 1741-1752.
Nascimento, E.A. & Del-Claro, K. (2010). Ant visitation to extrafloral nectaries decreases herbivory and increases fruit set in Chamaecrista debilis (Fabaceae) in a Neotropical savanna. Flora, 205: 754-756. doi: 10.1016/j.flora.2009.12.040
Nepi, M. (2007). Nectary structure and ultrastructure. In S.W. Nicolson, M. Nepi, & E. Pacini (Eds.), Nectaries and néctar (pp 129-166). Dordrecht, Springer.
Oliveira, O.S. & Leitão-Filho, H.F. (1987). Extrafloral Nectaries: Their taxonomic distribution and abundance in the woody flora of Cerrado vegetation in Southeast Brazil. Biotropica, 19: 140-148.
Oliveira, O.S. & Oliveira-Filho, A.T. (1991). Distribution of extrafloral nectarines in the woody flora of tropical communities in western Brazil. In P.W. Price, T.M. Lewin-Sohn, G.W. Fernandes & W.W. Benson (Eds.), Plant–animal interactions (pp 163-175). John Wiley and Sons, New York.
Orona-Tamayo, D., Wielsch, N., Escalante-Pérez, M., Svatos, A., MolinaTorres, J., Muck, A., Ramirez-Chávez, E., Ádame-Alvarez, R-M & Heil, M. (2013). Short-term proteomic dynamics reveal metabolic factory for active extrafloral nectar secretion by Acacia cornigera antplants. The Plant Journal, 73: 546-554. doi: 10.1111/tpj.12052
Paiva, E.A.S. & Machado, S.R. (2006). Ontogênese, anatomia e ultra-estrutura dos nectários extraflorais de Hymenaea stigonocarpa (Fabaceae-Caesalpinioideae). Acta Botanica Brasilica, 20: 471-482.
Rico-Gray, V. & Oliveira, P.S. (2007). The ecology and evolution of ant-plant interactions. University of Chicago Press, Chicago.
Rocha, J.F. & Machado, S.R. (2009). Anatomy, ultrastructure and secretion of Hibiscus pernambucensis Arruda (Malvaceae) extrafloral nectary. Revista Brasileira de Botânica, 32: 489-498. doi: 10.1590/S0100-84042009000300008
Sass, J.E. (1951). Botanical microtechique, 3°EDN. Iowa, State Press.
Schaffner, G. (1979). Extraflorale Nektarienbei Cuscuta. Berichte der Deutschen Botanischen. Gesellschaft, 92: 721-729.
Schaller, A. (2004). A cut above the rest: the regulatory function of plant proteases. Planta, 220: 183-197.
Stefani, V., Pires, T.L., Torezan-Silingardi, H.M. & Del-Claro, K. (2015). Beneficial effects of ants and spiders on the reproductive value of Eriothecagracilipes (Malvaceae) in a tropical savanna. PLoS ONE, 10(7): e0131843. doi: 10.1371/journal.pone.0131843
Stone, T.B., Thompson, A.C. & Pitre, H.N.(1985). Analysis of lipids in cotton extrafloral nectar. Journalof Entomological Science, 20:422-28.
Stpiczynska, M. & Davies, K.L. (2006). Nectary structure in Symphyglossum sanguineum (Rchb.f.) Schltr. (Orchidaceae).Acta Agrobotanica, 59: 7-16. 10.5586/aa.2006.001
Thadeo, M., Cassino, M.F., Vitarelli, N.C., Azevedo, A.A., Araújo, J.M., Valente, V.M.M. & Meira, R.M.S.A. (2008). Anatomical and histochemical characterization of extrafloral nectaries of Prockiacrucis (Salicaceae). American Journal of Botany, 95: 1515-1522. doi: 10.3732/ajb.0800120
Vilela, A.A., Torezan-Silingardi, H.M. & Del-Claro, K. (2014). Conditional outcomes in ant-plant-herbivore interactions influenced by sequential flowering. Flora, 209: 359-366. doi: 10.1016/j.flora.2014.04.004
Wagner, D. & Kay, A. (2002). Do extrafloral nectaries distract ants from visiting flowers? An experimental test of an overlooked hypothesis. Evolutionary Ecology Research, 4: 293-305.
Weber, M.G. & Keeler, K.H. (2013). The phylogenetic distribution of extrafloral nectaries in plants. Annals of Botany, 111: 1251-1261. doi: 10.1093/aob/mcs225
Weber, M.G., Porturas, L.D. & Keeler, K.H. (2015). World list of plants with extrafloral nectaries.www.extrafloralnectaries.org (acessed date: 23 September, 2016)
Wilder, S.M. & Eubanks, M.D. (2009). Extrafloral nectar content alters foraging preferences of a predatory ant. Biology Letters 6: 177-179. doi: 10.1098/rsbl.2009.0736
Wist, T.J. & Davis, A.R. (2006). Floral nectar production and nectary anatomy and ultrastructure of Echinacea purpurea (Asteraceae). Annals of Botany, 97: 177-193. doi: 10.1093/aob/mcj027
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).