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From species to individuals: does the variation in ant–plant networks scale result in structural and functional changes?

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Population Ecology

Abstract

Predicting the outcomes of any mutualistic interaction between ants and plants can be a very difficult task, since these outcomes are often determined by the ecological context in which the interacting species are embedded. Network theory has been an important tool to improve our understanding about the organizational patterns of animal–plant interactions. Nevertheless, traditionally, network studies have focused mainly on species-based differences and ignoring the importance of individual differences within populations. In this study, we evaluated if downscaling an ant–plant network from species to the individual level results in structural and functional changes in a network involving different-sized plant individuals. For this, we studied the extrafloral-nectar producing-tree Caryocar brasiliense (Caryocaraceae) and their associated ants in a Neotropical savanna. We observed 254 interactions involving 43 individuals of C. brasiliense and 47 ant species. The individual-based ant–plant network exhibited a nested pattern of interactions, with all developmental stages contributing equally to structuring this non-random pattern. We also found that plants with greater centrality within the network were better protected by their ant partners. However, plants with higher levels of individual specialization were not necessarily better protected by ants. Overall, we presented empirical evidence that intra-population variations are important for shaping ant–plant networks, since they can change the level of protection against herbivores conferred by the ants. These results highlight the importance of individual-based analyses of ecological networks, opening new research venues in the eco-evolutionary dynamics of ant–plant interactions.

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References

  • Almeida-Neto M, Guimarães P, Guimarães PR, Loyola RD, Urlich W (2008) A consistent metric for nestedness analysis in ecological systems: reconciling concept and measurement. Oikos 117:1227–1239

    Article  Google Scholar 

  • Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46

    Google Scholar 

  • Araujo MS, Guimaraes PR, Svanback R, Pinheiro A, Guimaraes P, dos Reis SF, Bolnick DI (2008) Network analysis reveals contrasting effects of intraspecific competitions on individual vs. population diets. Ecology 89:1981–1993

    Article  Google Scholar 

  • Araujo MS, Martins EG, Cruz LD, Fernandes FR, Linhares AX, dos Reis SF, Guimarães PR Jr (2010) Nested diets: a novel pattern of individual-level resource use. Oikos 119:81–88

    Article  Google Scholar 

  • Arruda FV, Pesquero MA, Marcelino DG, Leite GA, Delabie JHC, Fagundes R (2015) Size and condition of bamboo as structural factors behind the vertical stratification of the bamboo-nesting ant community. Insect Soc 63:99–107

    Article  Google Scholar 

  • Bascompte J, Jordano P (2006) The structure of plant-animal mutualistic networks. In: Pascual M, Dunne J (eds) Ecological networks. Oxford University Press, Oxford, pp 143–159

    Google Scholar 

  • Bascompte J, Jordano P (2013) Mutualistic networks. Princeton University Press, Princeton

    Book  Google Scholar 

  • Bascompte J, Jordano P, Melian CJ, Olesen J (2003) The nested assembly of plant-animal mutualistic networks. Proc Natl Acad Sci USA 100:9383–9387

    Article  CAS  Google Scholar 

  • Bastolla U, Fortuna MA, Pascual-García A, Ferrera A, Luque B, Bascompte J (2009) The architecture of mutualistic networks minimizes competition and increases biodiversity. Nature 458:1018–1021

    Article  CAS  Google Scholar 

  • Beattie A (1985) The evolutionary ecology of ant–plant mutualisms. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Benitez-Malvido J, Martínez-Falcón AP, Dattilo W, González-DiPierro AM, Lombera Estrada R, Traveset A (2016) The role of sex and age in the architecture of intrapopulation howler monkey–plant networks in continuous and fragmented rain forests. PeerJ 4:e1809

    Article  Google Scholar 

  • Blüthgen N, Fiedler K (2004) Competition for composition: lessons from nectar-feeding ant communities. Ecology 85:1479–1485

    Article  Google Scholar 

  • Blüthgen N, Verhaargh M, Goitía W, Jaffé K, Morawetz W, Barthott W (2000) How plants shape the ant community in the Amazonian rainforest canopy: the key role of extrafloral nectaries and homopteran honeydew. Oecologia 125:229–240

    Article  Google Scholar 

  • Blüthgen N, Menzel F, Blüthgen N (2006) Measuring specialization in species interaction networks. BMC Ecol 6:12–18

    Article  Google Scholar 

  • Bolnick DI, Svanback R, Fordyce JA, Yang LH, Davis JM, Hulsey CD, Forister ML (2003) The ecology of individuals: incidence and implications of individual specialization. Am Nat 161:1–28

    Article  Google Scholar 

  • Boudoris J, Queenborough SA (2013) Diversity and distribution of extra-floral nectaries in the cerrado savanna vegetation of Brazil. PeerJ 1:e219

    Article  Google Scholar 

  • Bronstein JL (1994) Conditional outcomes in mutualistic interactions. Trends Ecol Evol 9:214–217

    Article  CAS  Google Scholar 

  • Bronstein JL (1998) The contribution of ant plant protection studies to our understanding of mutualism. Biotropica 30:150–161

    Article  Google Scholar 

  • Bronstein JL, Alarcón R, Geber M (2006) The evolution of plant-insect mutualism. New Phytol 172:412–428

    Article  Google Scholar 

  • Camarota F, Powell S, Vasconcelos HL, Priest G, Marquis RJ (2015) Extrafloral nectaries have a limited effect on the structure of arboreal ant communities in a Neotropical savanna. Ecology 96:231–240

    Article  Google Scholar 

  • Camarota F, Powell S, Melo AS, Priest G, Marquis RJ, Vasconcelos HL (2016) Co-occurrence patterns in a diverse arboreal ant community are explained more by competition than habitat requirements. Ecol Evol 6:8907–8918

    Article  Google Scholar 

  • Cardoso E, Moreno MIC, Bruna EM, Vasconcelos HL (2009) Mudanças fitofisionômicas no Cerrado: 18 anos de sucessão ecológica na Estação Ecológica do Panga, Uberlândia - MG. Caminhos da Geografia 10:254–268 (in Portuguese)

    Google Scholar 

  • Chamberlain SA, Bronstein JL, Rudgers JA (2014) How context-dependent are species interactions. Ecol Lett 17:881–890

    Article  Google Scholar 

  • Dáttilo W (2012) Different tolerances of symbiotic and nonsymbiotic ant–plant networks to species extinctions. Netw Biol 2:127–138

    Google Scholar 

  • Dáttilo W, Guimarães PR, Izzo TJ (2013) Spatial structure of ant–plant mutualistic networks. Oikos 122:1643–1648

    Article  Google Scholar 

  • Dáttilo W, Fagundes R, Gurka CA, Silva MS, Vieira MC, Izzo TJ, Rico-Gray V (2014a) Individual-based ant–plant networks: diurnal-nocturnal structure and species-area relationship. PLoS One 9:e99838

    Article  Google Scholar 

  • Dáttilo W, Marquitti FMD, Guimarães PR, Izzo TJ (2014b) The structure of ant–plant ecological networks: is abundance enough? Ecology 95:475–485

    Article  Google Scholar 

  • Dáttilo W, Díaz-Castelazo C, Rico-Gray V (2014c) Ant dominance hierarchy determines the nested pattern in ant–plant networks. Biol J Linn Soc 113:405–414

    Article  Google Scholar 

  • Dáttilo W, Aguirre A, Flores-Flores R, Fagundes R, Lange D, García-Chavez J, Del-Claro K, Rico-Gray V (2015a) Secretory activity of extrafloral nectaries shaping multitrophic ant–plant–herbivore interactions in an arid environment. J Arid Environ 114:104–109

    Article  Google Scholar 

  • Dáttilo W, Aguirre A, Quesada M, Dirzo R (2015b) Tropical forest fragmentation affects floral visitors but not the structure of individual-based palm–pollinator networks. PLoS One 10:e0121275

    Article  Google Scholar 

  • Davidson DW, McKey D (1993) The evolutionary ecology of symbiotic ant–plant relationships. J Hymenopt Res 2:13–83

    Google Scholar 

  • Davidson DW, Cook SC, Snelling RR, Chua TH (2003) Explaining the abundance of ants in lowland tropical rainforest canopies. Science 300:969–972

    Article  CAS  Google Scholar 

  • Del-Claro K, Rico-Gray V, Torezan-Silingardi HM, Alves-Silva E, Fagundes R, Lange D, Dáttilo W, Vilela AA, Aguirre A, Rodríquez-Morales D (2016) Loss and gains in ant–plant interactions mediated by extrafloral nectar: fidelity, cheats, and lies. Insect Soc 63:207–221

    Article  Google Scholar 

  • Djiéto-Lordon C, Dejean A, Gibernau M, Hossaert-Mckey M, Mckey D (2004) Symbiotic mutualism with a community of opportunistic ants: protection, competition, and ant occupancy of the myrmecophyte Barteria nigritana (Passifloraceae). Acta Oecol 26:109–116

    Article  Google Scholar 

  • Dupont YL, Trøjelsgaard K, Olesen JM (2011) Scaling down from species to individuals: a flower-visitation network between individual honeybees and thistle plants. Oikos 120:170–177

    Article  Google Scholar 

  • Fagundes R, Dáttilo W, Ribeiro SP, Rico-Gray V, Del-Claro K (2016) Food source availability and interspecific dominance as structural mechanisms of ant–plant-hemipteran multitrophic networks. Arthropod Plant Interact 10:207–220

    Article  Google Scholar 

  • Fagundes R, Dáttilo W, Ribeiro SP, Rico-Gray V, Jordano P, Del-Claro K (2017) Differences between ant species in plant protection are influenced by the production of extrafloral nectar and related to the degree of leaf herbivory. Biol J Linn Soc 122:71–83

    Article  Google Scholar 

  • Falcão JCF, Dáttilo W, Izzo TJ (2014) Temporal variation in extrafloral nectar secretion in different ontogenic stages of the fruits of Alibertia verrucosa S. Moore (Rubiaceae) in a Neotropical savanna. J Plant Interact 9:137–142

    Article  Google Scholar 

  • Fiala B, Linsenmair KE (1995) Distribution and abundance of plants with extrafloral nectaries in the woody flora of a lowland primary forest in Malaysia. Biodivers Conserv 4:165–182

    Article  Google Scholar 

  • Floren A, Biun A, Linsenmair KE (2002) Arboreal ants as key predators in tropical lowland rainforest trees. Oecologia 131:137–144

    Article  Google Scholar 

  • Fonseca CR, Benson WW (2003) Ontogenetic succession in Amazonian ant trees. Oikos 102:407–412

    Article  Google Scholar 

  • Guimarães PR, Guimarães P (2006) Improving the analyses of nestedness for large sets of matrices. Environ Model Softw 21:1512–1513

    Article  Google Scholar 

  • Guimarães PR, Rico-Gray V, Dos Reis SF, Thompson JN (2006) Asymmetries in specialization in ant–plant mutualistic networks. Proc R Soc Lond B 273:2041–2047

    Article  Google Scholar 

  • Hagen M, Kissiling WD, Rasmussen C, Aguiar MAM, Brown DW, Carstensen DW, Alves-dos-Santos I, Dupont YL, Edwards FK, Genini J, Guimaraes PR, Jenkins GB, Jordano P, Kaiser-Bunbury CN, Ledger M, Maia KP, Marquitti FMD, McLaughlin O, Morellato LPC, O’Gorman EJ, Trojelsgaard K, Tylianakis JM, Vidal MM, Woodward G, Olesen J (2012) Biodiversity, species interactions and ecological networks in a fragmented world. Adv Ecol Res 46:89–210

    Article  Google Scholar 

  • Kersch MF, Fonseca CR (2005) Abiotic factors and the conditional outcome of an ant–plant mutualism. Ecology 86:2117–2126

    Article  Google Scholar 

  • Koch EBA, Camarota FC, Vasconcelos HL (2016) Plant ontogeny as a conditionality factor in the protective effect of ants on a Neotropical tree. Biotropica 48:198–205

    Article  Google Scholar 

  • Koptur S (2005) Nectar as fuel for plant protectors. In: Wäckers FL, Van Rijn PCJ (eds) Plant-provided food for carnivorous insects: a protective mutualism and its applications. Cambridge University Press, Cambridge, pp 75–108

    Chapter  Google Scholar 

  • Lee JH, Kim TW, Choe JC (2009) Commensalism or mutualism: conditional outcomes in a Branchiobdellid-crayfish symbiosis. Oecologia 159:217–224

    Article  Google Scholar 

  • Olesen JM, Dupont YL, O’Gorman EJ, Ings TC, Layer K, Melián CJ, Trøjelsgaard K, Pichler DE, Rasmussen C, Woodward G (2010) From broadstone to Zackenberg: space, time and hierarchies in ecological networks. Adv Ecol Res 42:1–69

    Article  Google Scholar 

  • Oliveira PS (1997) The ecological function of extrafloral nectaries: herbivore deterrence by visiting ants and reproductive output in Caryocar brasiliense (Caryocaraceae). Funct Ecol 11:323–330

    Article  Google Scholar 

  • Oliveira PS, Leitão-Filho HF (1987) Extrafloral nectaries: their taxonomic distribution and abundance in the woody flora of Cerrado vegetation in Southeast Brazil. Biotropica 19:140–148

    Article  Google Scholar 

  • Oliveira-Filho AT, Ratter JA (2002) Vegetation physiognomies and woody flora of the Cerrado biome. In: Oliveira PS, Marquis RJ (eds) The cerrados of Brazil. Columbia University Press, New York, pp 91–120

    Chapter  Google Scholar 

  • Pemberton RW (1998) The occurrence and abundance of plants with extrafloral nectaries, the basis for herbivore defensive mutualisms, along a latitudinal gradient in east Asia. J Biogeogr 25:651–668

    Article  Google Scholar 

  • Pires MM, Guimaraes PR, Aráujo MS, Giaretta AA, Costa JCL, dos Reis SF (2011) The nested assembly of individual-resource networks. J Anim Ecol 80:893–903

    Article  Google Scholar 

  • Powell S, Costa AN, Lopes CT, Vasconcelos HL (2011) Canopy connectivity and the availability of diverse nesting resources affect species coexistence in arboreal ants. J Anim Ecol 80:352–360

    Article  Google Scholar 

  • R Development Core Team (2017) R: a language and environment for statistical computing. r foundation for statistical computing. Vienna, Austria. http://www.r-project.org. Accessed Oct 2017

  • Rico-Gray V, Oliveira PS (2007) The ecology and evolution of ant–plant interactions. University of Chicago Press, Chicago

    Book  Google Scholar 

  • Rico-Gray V, Díaz-Castelazo C, Ramírez-Hernández A, Guimarães PR Jr, Holland JN (2012) Abiotic factors shape temporal variation in the structure of a mutualistic ant–plant network. Arthropod Plant Interact 6:189–295

    Article  Google Scholar 

  • Saavedra S, Stouffer DB, Uzzi B, Bascompte J (2011) Strong contributors to network persistence are the most vulnerable to extinction. Nature 478:233–235

    Article  CAS  Google Scholar 

  • Schoereder JH, Sobrinho TG, Madureira MS, Ribas CR, Oliveira PS (2010) The arboreal ant community visiting extrafloral nectaries in the Neotropical cerrado savanna. Terr Arthropod Rev 3:3–27

    Article  Google Scholar 

  • Thompson JN (2002) Plant–animal interactions: future directions. In: Herrera CM, Pellmyr O (eds) Plant–animal interactions. An evolutionary approach. Blackwell Science, Oxford, pp 236–247

    Google Scholar 

  • Tur C, Vigalondo B, Trøjelsgaard K, Olesen JM, Traveset A (2014) Downscaling pollen–transport networks to the level of individuals. J Anim Ecol 83:306–317

    Article  Google Scholar 

  • Vázquez D, Aizen MA (2003) Null model analyses of specialization in plant–pollinator interactions. Ecology 84:2493–2501

    Article  Google Scholar 

  • Vázquez D, Aizen MA (2004) Asymmetric specialization: a pervasive feature of plant–pollinator interactions. Ecology 85:1251–1257

    Article  Google Scholar 

  • Villamil N, Márquez-Guzmán J, Boege K (2013) Understanding ontogenetic trajectories of indirect defence: ecological and anatomical constraints in the production of extrafloral nectaries. Ann Bot Lond 112:1–9

    Article  Google Scholar 

  • Zamora R (1999) Conditional outcomes of interactions: the pollinator–prey conflict of an insectivorous plant. Ecology 80:786–795

    Google Scholar 

Download references

Acknowledgements

The authors would like to thank two anonymous reviewers for valuable comments on prior versions of this manuscript. This study was funded by research grants from the Brazilian Council of Research and Scientific Development (CNPq Grants 237339/2012-9 and 478107/2012-9), the Minas Gerais State Research Foundation (FAPEMIG), and the Brazilian Ministry for Education (MEC/CAPES).

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Authors and Affiliations

  1. Instituto de Biologia, Programa de Pós-graduação em Ecologia e Biomonitoramento, Universidade Federal da Bahia, Salvador, Bahia, Brazil

    Elmo B. A. Koch

  2. Instituto de Ecología A.C., Red de Ecoetología, Xalapa, Veracruz, Mexico

    Wesley Dáttilo

  3. Department of Biological Sciences, The George Washington University, Washington, DC, USA

    Flávio Camarota

  4. Instituto de Biologia, Universidade Federal de Uberlândia (UFU), Uberlândia, Minas Gerais, Brazil

    Heraldo L. Vasconcelos

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  1. Elmo B. A. Koch
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  2. Wesley Dáttilo
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Correspondence to Elmo B. A. Koch.

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Koch, E.B.A., Dáttilo, W., Camarota, F. et al. From species to individuals: does the variation in ant–plant networks scale result in structural and functional changes?. Popul Ecol 60, 309–318 (2018). https://doi.org/10.1007/s10144-018-0634-5

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