Effects of ants on pollinator performance in a distylous pericarpial nectary-bearing Rubiaceae in Brazilian Cerrado

Bruno de Sousa-Lopes, Eduardo Soares Calixto, Eduardo Soares Calixto, Helena Maura Torezan-Silingardi, Helena Maura Torezan-Silingardi, Kleber Del-Claro, Kleber Del-Claro

Abstract


Besides the eff ectiveness of floral visitors, to better understand pollination systems is necessary to consider the role of predators. Ants are ubiquitous on the vegetation, especially on plants bearing extrafloral (EFNs) and pericarpial nectaries (PNs). Both EFNs and PNs reward ants which in turn provide to plants effective protection against herbivores. However, ants can also repel pollinators and cause an indirect cost for the plant partner, although the role of ants on pollinators’ performance has rarely been assessed in Neotropics, mainly on PN-bearing plants. Here, our main aim was, through an experimental field study in terms of ant’s presence versus absence, to test the hypothesis that ants dissuade floral visitors by decreasing the time spent during visits on the PN-bearing Declieuxia fruticosa. Additionally, we recorded floral phenology, and quantified and qualified floral visits. We showed that bees were the most frequent pollinators and the presence of ants dissuades them. In ant presence, pollinators were on average 30% faster than without ants. Since D. fruticosa produces fruits mainly after cross-pollination, the role of ants may be profi table to plants as they induce pollinators to do shorter visits and search for other fl owers in conspecifi c plants. Therefore, pollinators avoid stay at longer on plants with ants in order to avoid attacks, which may contribute to plant outcrossing. However, whether positive or negative the effects of ants on D. fruticosa reproduction are, they remain to be studied.


Keywords


Apis mellifera; Brazilian Cerrado; Ectatoma brunneum; entomophily; Insect-plant interactions

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References


ALMEIDA-SOARES S, POLATTO LP, DUTRA JCS & TOREZAN-SILINGARDI HM (2010). Pollination of Adenocalymma bracteatum (Bignoniaceae): Floral Biology and Visitors. Neotropical Entomology 39(6):941–948.

ALTMANN J (1974) Observational study of behavior: sampling methods. Behaviour 48:227–267.

ALVES-DOS-SANTOS I, SILVA CI, PINHEIRO M & KLEINERT AMP (2016) When a floral visitor is a pollinator? Rodriguésia 67(2):295–307 .

ARAÚJO GM, BARBOSA AAA, ARANTES AA & AMARAL AF (2002) Composição florística de veredas no município de Uberlândia, MG. Revista Bras. Bot. 25(4):475–493.

ASSUNÇÃO MA, TOREZAN-SILINGARDI HM & DEL-CLARO K (2014) Do ant visitors to extrafloral nectaries of plants repel pollinators and cause an indirect cost of mutualism? Flora 09:244–249.

BÄCHTOLD A, ALVES-SILVA E & DEL-CLARO K (2017) Ant-related oviposition is not associated to low parasitism of the myrmecophilous butterfly Allosmaitia strophius in an extrafloral nectaried shrub. Acta Oecologica 83:15–21.

BARRETT SCH (1992) Evolution and function of heterostyly. Springer-Verlag, Berlin.

BARRETT SCH & RICHARDS JH (1990) Heterostyly in tropicalplants. Memoirs of New York Botanical Garden 55:35–61.

CALIXTO ES, LANGE D & DEL-CLARO K (2018) Protection mutualism: an overview of ant-plant interactions mediated by extrafloral nectaries. Oecologia Aust 22:410–425. doi: 10.4257/oeco.2018.2204.05

CARRECK N & WILLIAMS I (1998) The economic value of bees in the UK. Bee World 79(3):115–23.

CLEMENTE MA, LANGE D, DEL-CLARO K, PREZOTO F, CAMPOS NR & BARBOSA BC (2012) Flower-visiting social wasps and plants interaction: network pattern and environmental complexity. Psyche: The Journal of Entomology 2012:1–10.

COELHO CP & BARBOSA AAA (2003) Reproductive biology of Palicourea macrobotrys Ruiz & Pavon (Rubiaceae): a possible case of homostyly in the genus Palicourea Aubl. Revista Brasil. Bot. 26(3):403–413.

COELHO CP & BARBOSA AAA (2004) Reproductive biology of Psychotria poeppigiana Mull. Arg. (Rubiaceae) in gallery forest. Acta bot. bras 18(3):481–489.

CREPET WL (1984) Advanced (constant) insect pollination mechanisms: pattern of evolution and implications vis-a´-vis angiosperm diversity. Ann Mo Bot Gard 71: 607–630.

DAFNI A & MAUÉS MM (1998) A rapid and simple procedure to determine stigma receptivity. Sex Plant Reprod 11:177–180. doi: 10.1007/s004970050138

DEL-CLARO K, RICO-GRAY V, TOREZAN-SILINGARDI HM, ALVES-SILVA, E., FAGUNDES, R., LANGE, D., DÁTILLO, 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 Soc 63:207–221. doi: 10.1007/s00040-016-0466-2.

DEL-CLARO K, GUILLERMO-FERREIRA R, ALMEIDA EM, ZARDINI H & TOREZAN-SILINGARDI HM (2013) Ants Visiting the Post-Floral Secretions of Pericarpial Nectaries in Palicourea rigida (Rubiaceae) Provide Protection Against Leaf Herbivores But Not Against Seed Parasites. Sociobiology doi:10.13102/sociobiology.v60i3.217-221. 60:217–221.

DELPRETE PG (2010) Flora dos estados de Goiás e Tocantins. Gráfica e Editora Vieira Goiânia. 1610p.

DICKS LV, ABRAHAMS A, ATKINSON J, BIESMEIJER J, BOURNE N, BROWN C, BROWN MJF, CARVELL C, CONNOLLY C, CRESSWELL JE, CROFT P, DARVILL B, DE ZYLVA P, EFfiNGHAM P, FOUNTAIN M, GOGGIN A, HARDING D, HARDING T, HARTfiELD C, HEARD MS, HEATHCOTE R, HEAVER D, HOLLAND J, HOWE M, HUGHES B, HUXLEY T, KUNIN WE, LITTLE J, MASON C, MEMMOTT J, OSBORNE J, PANKHURST T, PAXTON RJ, POCOCK MJO, POTTS SG, POWER EF, RAINE NE, RANELAGH E, ROBERTS S, SAUNDERS R, SMITH K, SMITH RM, SUTTON P, TILLEY LAN, TINSLEY A, TONHASCA A, VANBERGEN AJ, WEBSTER S, WILSON A & SUTHERLAND WJ (2013) Identifying key knowledge needs for evidence-based conservation of wild insect pollinators: a collaborative cross-sectoral exercise. Insect Conserv Divers 6:435–446.

DORMANN CF, FRUND J, BLUTHGEN N & GRUBER B (2009) Indices, graphs and null models: analyzing bipartite ecological networks. Open Ecol J 2:7–24. DOI: 10.2174/1874213000902010007.

FERREIRA CA & TOREZAN-SILINGARDI HM (2013) Implications of the floral herbivory on Malpighiaceae plant fitness: visual aspect of the flower affects attractiveness to pollinators. Sociobiology 60:217–221.

GALEN C & NEWPORT MEA (1987) Bumble bee behavior and selection on flower size in the sky pilot, Polemonium viscosum. Oecologia 74:20–23.

GRIMALDI D (1999) The co-radiations of pollinating insects and angiosperms in the Cretaceous. Ann Mo Bot Gard 86:373–406.

HAMILTON CW (1990) Variation on a distylous Theme in Mesoamerican Psychotria subgenus Psychotria (Rubiaceae). Memoirs of the New York Botanical Garden 55:62–75.

HERRERA CM (1989) Pollinator abundance, morphology, and flower visitation rate: Analysis of the “quantity” component in a plant-pollinator system. Oecologia 80:241–248.

KOPTUR S (1992) Extrafloral nectary-mediated interactions between insects

and plants. In: BERNAYS E (ed) Insect-Plant Interactions. CRC Press, Boca raton, pp 81–129.

MALOOF JE (2001) The effects of a bumble bee nectar robber on plant reproductive success and pollinator behavior. American Journal of Botany 88(11):1960–1965.

MATIAS R, OLIVEIRA AS, FURTADO MT, SÁ T, RODRIGUES EB, OLIVEIRA PE & CANSOLARO H (2016) Atypical mating system in two Rubiaceae species: distyly with partial self-incompatibility in the thrum morph? Rodriguesia 67:357–368.

MAYEFIELD MM, WASER NM & PRICE MV (2001) Exploring the ‘Most Effective Pollinator Principle’ with Complex Flowers: Bumblebees and Ipomopsis aggregate. Ann Bot. 88(4):591–596. DOI: 10.1006/anbo.2001.1500.

MILO R, SHEN-ORR S, ITZKOVITZ S, KASHTAN N, CHKLOVSKII D & ALON U (2002) Network Motifs: simple building blocks of complex networks. Science 298 (5594):824–827. DOI: 10.1126/science.298.5594.824.

NESS JH (2006) A mutualism’s indirect costs: The most aggressive plant bodyguards also deter pollinators. Oikos 113:506–514. doi: 10.1111/j.2006.0030-1299.14143.x

OLSEN KM (1997) Pollination eectiveness and pollinator importance in a population of Heterotheca subaxillaris (Asteraceae). Oecologia 109:114–121.

PAILLER T & THOMPSON JD (1997) Distyly and variation in heteromorphic incompatibility in Gaertnera vaginata (Rubiaceae) endemic to La Reunion Island. American Journal of Botany 84:315–327.

POTTS SG, BIESMEIJER JC, KREMEN C, NEIMANN P, SCHWEIGER O & KUNIN WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353.

R DEVELOPMENT CORE TEAM. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available in: . Accessed: 10 Oct. 2015.

SAEED S, NAQQASH MN, JALEEL W, SAEED Q & GHOURI F (2016) Effect of the blowflies (Diptera: Calliphoridae) on the size and weight of Mango (Mangifera indica L.). PeerJ PrePrints 4:e1683v1.

SANTOS JC & DEL-CLARO K (2001) Interactions between ants, herbivores and extrafloral nectaries in Tocoyena Formosa (Cham. & Schlechtd.) K. Schum. (Rubiaceae) in Cerrado vegetation. Revista Brasileira de Zoociências 3:77–92.

SHUTTLEWORTH A & JOHNSON SD (2009) The importance of scent and nectar filters in a specialized wasp-pollination system. Functional Ecology 23:931–940.

THOMPSON JN (1997) Conserving interaction biodiversity. In: PICKETT STA, OSTFELD RS, SHACHAK M & LIKENS GE (eds) The ecological basis of conservation: Heterogeneity, ecosystems, and biodiversity. Chapman & Hall, New York, pp 285–293.

TYLIANAKIS JM, LALIBERTÉ E, NIELSEN A & BASCOMPTE J (2010) Conservation of species interaction networks. Biological Conservation 143: 2270–2279.

VILLAMIL N, BOEGE K & STONE GN (2018) Ant-pollinator conflict results in pollinator deterrence but no nectar trade-offs. Front Plant Sci 9:1–14. DOI: 10.3389/fpls.2018.01093.

VILELA AA, TOREZAN-SILINGARDI HM & DEL-CLARO K (2014) Conditional outcomes in ant–plant–herbivore interactions influenced by sequential flowering. Flora 209(7):359–366.

VILELA AA, CLARO VTS, TOREZAN-SILINGARDI HM & DEL-CLARO K (2018) Climate changes affecting biotic interactions, phenology, and reproductive success in a savanna community over a 10-year period. Arthropod-Plant Interactions. DOI 10.1007/s11829-017-9572-y-2018.

WARDHAUGH CW (2015) How many species of arthropods visit flowers? Arthropod-Plant Interactions 9:547–565.

WARDHAUGH CW, STORK, NE, EDWARDS W & GRIMBACHER PS (2013) Insects on flowers: The unexpectedly high biodiversity of flower-visiting beetles in a tropical rainforest canopy. Communicative & Integrative Biology 6:1,e22509.

WEBER MG & KEELER KH (2013) The phylogenetic distribution of extrafloral nectaries in plants. Ann Bot 111:1251–1261. DOI: 10.1093/aob/mcs225.




DOI: http://dx.doi.org/10.13102/sociobiology.v67i2.4846

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