Protection of Vochysia elliptica (Vochysiaceae) by a nectar-thieving ant

Proteção de Vochysia elliptica (Vochysiaceae) por uma formiga que rouba néctar

Abstracts

Vochysia elliptica (Vochysiaceae) is a shrubby plant, which does not have EFNs. Camponotus ants thieve nectar, and can decrease plant fitness by making flowers less attractive to pollinators. However, ants remove herbivores, wich can be beneficial. Results show that plants from which ants were excluded had lower rates of termite (simulated herbivore) removal than did plants visited by ants. Plants accessible to ants showed higher rates of termite removal in the base of leaves and in the inflorescence, than in the tip of leaves. This occurs because ants must pass through the principal axis to reach the inflorescence. Conclusive results of this cost/benefit analysis of the Camponotus sp. presence for V. elliptica can be obtained, with experimental manipulations.

ant-plant interaction; flower nectar; plant protection; rupestrian field; Vochysia elliptica


Vochysia elliptica (Vochysiaceae) é uma planta arbustiva que não porta NEFs. Formigas Camponotus roubam néctar e podem diminuir a aptidão da planta, tornando as flores menos atrativas para polinizadores. O efeito das formigas na remoção dos herbívoros, no entanto, pode ser benéfico. Resultados evidenciaram que plantas cujas formigas foram excluídas tiveram menor taxa de remoção de cupins (herbívoros simulados) do que plantas visitadas por formigas. Plantas com acesso às formigas apresentaram maior taxa de cupins removidos na base das folhas e na inflorescência do que na ponta das folhas. Isso ocorre porque formigas devem passar através do eixo principal para alcançar a inflorescência. Resultados conclusivos dessa análise de custo/benefício da presença de Camponotus sp. para V. elliptica deverão ser obtidos no futuro, com manipulações experimentais.

campo rupestre; interação formiga-planta; néctar floral; proteção da planta; Vochysia elliptica


Notes and Comments

PROTECTION OF Vochysia elliptica (VOCHYSIACEAE) BY A NECTAR-THIEVING ANT

ROMERO, G. Q.

Pós-graduação em Ecologia, Departamento de Zoologia, Universidade Estadual de Campinas, Unicamp, C.P. 6109, CEP 13081-970, Campinas, SP, Brazil

Correspondence to: Gustavo Q. Romero, Rua 14 de dezembro, 55, apto. 509, Centro, CEP 13015-919, Campinas, SP, Brazil, e-mail: gqromero@unicamp.br

Received December 18, 2000 ¾ Accepted September 13, 2001 ¾ Distributed May 31, 2002

(With 1 figure)

ABSTRACT

Vochysia elliptica (Vochysiaceae) is a shrubby plant, which does not have EFNs. Camponotus ants thieve nectar, and can decrease plant fitness by making flowers less attractive to pollinators. However, ants remove herbivores, wich can be beneficial. Results show that plants from which ants were excluded had lower rates of termite (simulated herbivore) removal than did plants visited by ants. Plants accessible to ants showed higher rates of termite removal in the base of leaves and in the inflorescence, than in the tip of leaves. This occurs because ants must pass through the principal axis to reach the inflorescence. Conclusive results of this cost/benefit analysis of the Camponotus sp. presence for V. elliptica can be obtained, with experimental manipulations.

Key words: ant-plant interaction, flower nectar, plant protection, rupestrian field, Vochysia elliptica.

RESUMO

Proteção de Vochysia elliptica (Vochysiaceae) por uma formiga que rouba néctar

Vochysia elliptica (Vochysiaceae) é uma planta arbustiva que não porta NEFs. Formigas Camponotus roubam néctar e podem diminuir a aptidão da planta, tornando as flores menos atrativas para polinizadores. O efeito das formigas na remoção dos herbívoros, no entanto, pode ser benéfico. Resultados evidenciaram que plantas cujas formigas foram excluídas tiveram menor taxa de remoção de cupins (herbívoros simulados) do que plantas visitadas por formigas. Plantas com acesso às formigas apresentaram maior taxa de cupins removidos na base das folhas e na inflorescência do que na ponta das folhas. Isso ocorre porque formigas devem passar através do eixo principal para alcançar a inflorescência. Resultados conclusivos dessa análise de custo/benefício da presença de Camponotus sp. para V. elliptica deverão ser obtidos no futuro, com manipulações experimentais.

Palavras-chave: campo rupestre, interação formiga-planta, néctar floral, proteção da planta, Vochysia elliptica.

Floral nectaries are attractive to pollinators, whereas extrafloral nectaries (EFNs) attract predators, such as ants and wasps, which attack herbivores and can increase plant fitness. However, some authors identify ants and wasps which visit floral nectaries and can be useful in fighting plant herbivores (Dominguez et al., 1989; Yano, 1994).

Vochysia elliptica Mart. (Vochysiaceae) is a shrubby plant that lacks EFNs (Stafleu, 1948, 1952). The leaves are about 5.0 cm in length, and have a very short petiole. Each branch has only one inflorescence at the apex. The floral nectar is produced and stored in the spur, which is a derived structure of the calyx located in the frontal region of the flower (Oliveira & Gibbs, 1994: Fig. 2). An ant species, Camponotus sp., visits the flowers of Vochysia elliptica and thieves nectar from the upper part of the spurs (G. Romero, unpubl.) which was probably previously perforated by wasps and/or bees (Young, 1980). The ants in effect act like opportunists by making the flowers less attractive to pollinators. On the other hand, preliminary observations showed that these thievish ants remove herbivores from flowers and leaves. To analyze the behaviour of Camponotus sp. and its effect on the fitness of V. elliptica, I first attempted to discover, by a simple field experiment, if this ant can remove the herbivores from V. elliptica.

Field work was undertaken in rupestrian vegetation (Menezes & Giulietti, 1986) in the Cipó Mountain (1300 m alt.), Minas Gerais State, Southeastern Brazil (43°35'W, 19°17'S) in May (dry season), 1998.

Twenty-four shrubs of V. elliptica ranging from 0.5 to 1.6 m in height were randomly chosen within a plot of about 0.3 ha. Each plant had at least two branches with inflorescence. After removing all ants and other insect species from these branches, ten live termite workers were glued as models of natural herbivores (Oliveira et al., 1987a, b; Freitas & Oliveira, 1996), with non-toxic Cascolarâ glue, at the following locations; 1) at the top and 2) base of the leaves, and 3) in the inflorescence. One branch was isolated at the base (about 10 cm above the ground) with Tanglefootâ resin to hinder recruitment by ants (control group), while the other branch was not isolated (experimental group). All other vegetation that was more than 10 cm in height was removed in the control group to avoid the approach of ants.

The removal rates of termites by ants were evaluated 24 h after attaching the workers. After testing normality and variance homogeneity, the removal rates were compared using the two-way ANOVA test followed by the Bonferroni a posteriori test (Sokal & Rohlf, 1981).

The results of the field experiment are shown in Fig. 1. The mean number of termites removed was significantly higher in the three experimental groups (at the top, base of leaves, and inflorescence) than in the control group (ANOVA, F = 1935.3, p < 0.0001). The removal rate of termites in experimental groups was significantly higher at the base than at the top of the leaves (ANOVA/Bonferroni, t = 3.24, p < 0.05), while no significant difference was observed between the top of the leaves and inflorescence (ANOVA/Bonferroni, t = 1.49, p > 0.05) and between the base of the leaves and inflorescence (ANOVA/Bonferroni, t = 1.75, p > 0.05).

The results suggests that Camponotus sp. can potentially protect V. elliptica from herbivores. The higher rates of removal at the base of leaves and inflorescences seem to be related to the foraging route of ants via the principal axis towards the inflorescences. During this field experiment, up to twelve individuals of Camponotus sp. climbed the stem of V. elliptica and reached the inflorescences. Some of these individuals thieved nectar.

The elimination of herbivores from flowers, fruits, and seeds by ants has a beneficial effect on plants (Schemske, 1980; Stephenson, 1982; Del-Claro et al., 1996; Oliveira et al., 1999). Moreover, some ant species also play an important role in pollination (Harber et al., 1981). On the other hand, nectar thief behaviour reduces the reproductive success of plants either because they become less attractive for pollinators (Galen, 1983; Irwin & Brody, 1998), or because the presence of the predator in the inflorescences can interfere with the foraging behaviours of pollinators (Bristowe, 1958; Elliott & Elliott, 1991). However, since the data suggested that Camponotus sp. can potentially benefit on V. elliptica, a cost/benefit analysis involving experimental manipulation to examine herbivory and pollination rates, is needed to better understand this ant-plant interaction.

Acknowledgments — I thank Dr. J. R. Trigo, Departamento de Zoologia, Unicamp, for helpful suggestions and statistical analysis. Drs. S. Nakano of Hiroshima Shudo University; P. S. Oliveira of the Departamento de Zoologia, Unicamp; and D. de C. Rossa-Feres, Departamento de Zoologia, Unesp, São José do Rio Preto, read and commented on the manuscript. I am grateful to K. P. Calligaris, S. C. Barão, W. Jesus, A. W. Jannini, and A. J. Santos for help in the field.

  • BRISTOWE, W. S., 1958, The world of spiders Collins, London, 304p.
  • DEL-CLARO, K., BERTO, V. & RÉU, W., 1996, Effect of herbivore deterrence by ants on the fruit set of an extrafloral nectary plant, Qualea multiflora (Vochysiaceae). Journal of Tropical Ecology, 12: 887-892.
  • DOMINGUEZ, C. A., DIRZO, R. & BULLOCK, S. H., 1989, On the function of floral nectar in Croton suberosus (Euphorbiaceae). Oikos, 56: 109-114.
  • ELLIOTT, N. B. & ELLIOTT, W. M., 1991, Effect of an ambush predator, Phymata americana Melin, on behavior of insects visiting Daucus carota American Midland Naturalist, 126: 198-202.
  • FREITAS, A. V. L. & OLIVEIRA, P. S., 1996, Ants as selective agents on herbivore biology: effects on the behaviour of a non-myrmecophilous butterfly. Journal of Animal Ecology, 65: 205-210.
  • GALEN, C., 1983, The effects of nectar thieving ants on seedset in floral scent morphs of Polemonium viscosum Oikos, 41: 245-249.
  • HABER, W. A., FRANKIE, G. W., BAKER, H. G. & KOPTUR, S., 1981, Ants like flower nectar. Biotropica, 13: 211-214.
  • IRWIN, R. E. & BRODY, A. K., 1998, Nectar robbing in Ipomopsis aggregata: effects on pollinator behavior and plant fitness. Oecologia, 116: 519-527.
  • MENEZES, N. L. & GIULIETTI, A. M., 1986, Campos rupestres. Ciência Hoje, 5: 38-47.
  • OLIVEIRA, P. & GIBBS, P., 1994, Pollination biology and breeding systems of six Vochysia species (Vochysiaceae) in central Brazil. Journal of Tropical Ecology, 10: 509-522.
  • OLIVEIRA, P. S., OLIVEIRA-FILHO, A. T. & CINTRA, R., 1987a, Ant foraging on ant-inhabited Triplaris (Polygonaceae) in western Brazil: a field experiment using live termite-baits. Journal of Tropical Ecology, 3: 193-200.
  • OLIVEIRA, P. S., SILVA, A. F. & MARTINS, A. B., 1987b, Ant foraging on extrafloral nectaries of Qualea grandiflora (Vochysiaceae) in cerrado vegetation: ants as potential antiherbivore agents. Oecologia, 74: 228-230.
  • OLIVEIRA, P. S., RICO-GRAY, V., DÍAZ-CASTELAZO, C. & CASTILLO-GUEVARA, C., 1999, Interaction between ants, extrafloral nectaries and insect herbivores in neotropical coastal sand dunes: herbivore deterrence by visiting ants increases fruit set in Opuntia stricta (Cactaceae). Functional Ecology, 13: 623-631.
  • SCHEMSKE, D. W., 1980, The evolutionary significance of extrafloral nectar production by Costus woodsonii (Zingiberaceae): an experimental analysis of ant protection. Journal of Ecology, 68: 959-967.
  • SOKAL, R. R. & ROHLF, F. J., 1981, Biometry 2nd ed., Freeman, San Francisco, 859p.
  • STAFLEU, F. A., 1948, A monography of the Vochysiaceae. I. Salvertia and Vochysia Mededelingen van het Botanisch Museum en Herbarium van de Rijksuniversiteit te Utrecht, 95: 379-450.
  • STAFLEU, F. A., 1952, A monography of the Vochysiaceae. II. Callisthene Acta Botanica Neerlandica, 1: 222-242.
  • STEPHENSON, A. G., 1982, The role of the extrafloral nectaries of Catalpa speciosa in limiting herbivory and increasing fruit production. Ecology, 63: 663-669.
  • YANO, S., 1994, Flower nectar of an autogamous perennial Rorippa indica as an indirect defense mechanism against herbivorous insects. Researches on Population Ecology, 36: 63-71.
  • YOUNG, A. M., 1980, Nectar robbing of "Four-o-clocks", Mirabilis jalapa (Nyctaginaceae) by the social wasp Epipona guerini (Vespidae) in Costa Rica. Biotropica, 12: 222-223.

Publication Dates

  • Publication in this collection
    26 Aug 2002
  • Date of issue
    May 2002

History

  • Accepted
    13 Sept 2001
  • Received
    18 Dec 2000
Instituto Internacional de Ecologia R. Bento Carlos, 750, 13560-660 São Carlos SP - Brasil, Tel. e Fax: (55 16) 3362-5400 - São Carlos - SP - Brazil
E-mail: bjb@bjb.com.br