A New Extrafloral Nectary-Bearing Plant Species in the Brazilian Savanna and its Associated Ant Community: Nectary Structure, Nectar Production and Ecological Interactions

Authors

  • Marcela Saldanha Pires Universidade Federal de Uberlândia
  • Eduardo S Calixto Universidade de São Paulo, FFCLRP, Ribeirão Preto
  • Denis C Oliveira Universidade Federal de Uberlândia
  • Kleber Del-Claro Universidade Federal de Uberlândia http://orcid.org/0000-0001-8886-9568

DOI:

https://doi.org/10.13102/sociobiology.v64i3.1603

Keywords:

ants, mutualism, extrafloral nectaries

Abstract

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

Download data is not yet available.

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

2017-10-17

How to Cite

Pires, M. S., Calixto, E. S., Oliveira, D. C., & Del-Claro, K. (2017). A New Extrafloral Nectary-Bearing Plant Species in the Brazilian Savanna and its Associated Ant Community: Nectary Structure, Nectar Production and Ecological Interactions. Sociobiology, 64(3), 228–236. https://doi.org/10.13102/sociobiology.v64i3.1603

Issue

Section

Research Article - Ants

Most read articles by the same author(s)

1 2 > >>