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Influence of grazing intensity on patterns and structuring processes in plant–pollinator networks in a subtropical grassland

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Abstract

Understanding how disturbances influence interaction networks is a central but still poorly explored issue in ecology and management. The goal of this study was to test how the structure of plant–pollinator networks and the structuring processes are influenced by grazing in a subtropical grassland community on the southern hemisphere. Twelve sampling plots were allocated in order to cover a grazing gradient ranging from overgrazed to ungrazed sites. For each plot, we created a quantitative matrix containing all observed pairwise insect–plant interactions and described morphology, phenology and abundances of each species. We fitted a series of models to test the influence of grazing intensity on metrics describing networks structure. We finally used probabilistic matrices, maximum likelihood and model selection to investigate the processes influencing frequencies of interactions across the gradient of disturbance. Grazing intensity influenced connectance, specialization and interaction evenness, while the number of species and links, nestedness and modularity were less variable. Species abundance was the most important determinant of interaction frequencies regardless of grazing intensity. In contrast to northern hemisphere pollination networks studied so far, these subtropical plant–pollinator networks and their structuring processes were remarkably consistent along the grazing gradient. We argue that this results from the dominance of generalist Asteraceae species, which are selectively avoided by cattle and play a core role in attracting a wide range of pollinators and thereby structuring plant–pollinator interactions, providing therefore stability.

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References

  • Adler P, Lauenroth W (1998) The effect of grazing on the spatial heterogeneity of vegetation. Oecologia 4:465–479

    Google Scholar 

  • Aizen AM, Feisinger P (1994) Forest fragmentation, pollination, and plant reproduction in a Chaco dry forest, Argentina. Ecology 75:330–351

    Article  Google Scholar 

  • Almeida-Neto M, Ulrich W (2011) A straightforward computational approach for measuring nestedness using quantitative matrices. Environ Model Softw 26:173–178

    Article  Google Scholar 

  • Andrade BO, Bonilha CL, Overbeck GE et al (2019) Classification of South Brazilian grasslands: implications for conservation. Appl Veg Sci 1:1–10. https://doi.org/10.1111/avsc.12413

    Article  Google Scholar 

  • Antonini Y, Martins RP (2003) The flowering- visiting bees at the Ecological Station of the Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil. Neotrop Entomol 32:565–575

    Article  Google Scholar 

  • Ashman TL, King EA (2005) Are flower-visiting ants mutualists or antagonists? A study in a gynodioecious wild strawberry. Am J Bot 92:891–895

    Article  PubMed  Google Scholar 

  • Baker DL, Guthery ES (1990) Effects of continuous grazing on habitat and density of ground-foraging birds in south Texas. J Range Manag 43:2–5

    Article  Google Scholar 

  • Baldissera R, Fritz L, Rauber R, Muller SC (2010) Comparison between grassland communities with and without disturbances. Neotrop Biol Conserv 5:3–10

    Article  Google Scholar 

  • Bascompte J, Jordano P (2007) Plant-Animal Mutualistic Networks: the Architecture of Biodiversity. Ann Rev Ecol Evol Syst 38:567–593

    Article  Google Scholar 

  • Bascompte J, Jordano P, Melián CJ, Olesen JM (2003) The nested assembly of plant–animal mutualistic networks. PNAS 100(16):9383–9387

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bascompte J, Jordano P, Olesen JM (2006) Asymmetric coevolutionary networks facilitate biodiversity maintenance. Science 312:431–433

    Article  CAS  PubMed  Google Scholar 

  • Basilio AM, Medan D, Torreta JP, Bartoloni NJ (2006) A year-long plant-pollinator network. Austral Ecol 31:975–983

    Article  Google Scholar 

  • Bastazini VAG, Ferreira PMA, Azambuja BO, Casas G, Debastiani VJ, Guimarães PR, Pillar VD (2017) Untangling the tangled bank: a novel method for partitioning the effects of phylogenies and traits on ecological networks. Evol Biol 44:312–324

    Article  Google Scholar 

  • Ben Bolker and R Development Core Team (2014) bbmle: Tools for general maximum likelihood estimation. R package version 1.0.17. http://CRAN.R-project.org/package=bbmle

  • Beretta ME, Fernandes AC, Schneider AA, Ritter MR (2008) A família Asteraceae no Parque Estadual de Itapuã, Viamão, Rio Grande do Sul, Brasil. Braz J Biosci 6:189–216

    Google Scholar 

  • Blancafort X, Gómez C (2005) Consequences of the Argentine ant, Linepithema humile (Mayr), invasion on pollination of Euphorbia characias (L.) (Euphorbiaceae). Oecologia 28:49–55

    Article  Google Scholar 

  • Blüthgen N, Fründ J, Vásquez DP, Menzel F (2008) What do interaction networks metrics tell us about specialization and biological traits? Ecology 89:3387–3399

    Article  PubMed  Google Scholar 

  • Boldrini II, Eggers L (1996) Vegetação campestre do sul do Brasil: resposta e dinâmica de espécies à exclusão. Acta Bot Bras 10:37–50

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference, 2nd edn. Springer, New York

    Google Scholar 

  • Cingolani AM, Posse G, Collantes MB (2005) Plant functional traits, herbivore selectivity and response to sheep grazing in Patagonian steppe grasslands. J Appl Ecol 42:50–59

    Article  Google Scholar 

  • Costanza R, d’Arge R, Groot R, Farberk S, Grasso M, Hannon B, Limburg K, Naeem S, O’Neill RV, Paruelo J, Raskin RG, Suttonkk P, Van den Belt M (1997) The value of the world’s ecosystem services and natural capital. Nature 387:253–260

    Article  CAS  Google Scholar 

  • Cruz CEF, Karam FC, Dalto AC, Pavarini SP, Bandarra PM, Driemeier D (2010) Fireweed (Senecio madagascariensis) poisoning in cattle. Pesquisa Veterinária Brasileira https://doi.org/10.1590/s0100-736x2010000100002.

  • Dalsgaard B, Schleuning M, Maruyama PK, Dehling DM, Sonne J, Vizentin-Bugoni J, Zanata TB, Fjeldså J, Böhning-Gaese K, Rahbek C (2017) Opposed latitudinal patterns of network-derived and dietary specialization in avian plant–frugivore interaction systems. Ecography 40:1395–1401

    Article  Google Scholar 

  • Develey PF, Setubal RB, Dias RA, Bencke GA (2008) Conservação das aves e da biodiversidade no bioma pampa aliada a sistemas de produção animal. Rev Bras Ornitol 16:308–315

    Google Scholar 

  • Dias et al (2017) Livestock disturbance in Brazilian grasslands influences avian species diversity via turnover. Biodivers Conserv 226:2473–2490

    Article  Google Scholar 

  • Dorman CF, Strauss R (2014) A method for detecting modules in quantitative bipartite networks. Methods Ecol Evol 5:90–98

    Article  Google Scholar 

  • Dorman CF, Gruber B, Frund J (2008) Introducing the bipartite package: analysing ecological networks. R News 8:8–11

    Google Scholar 

  • Dutton EM, Frederinckson ME (2012) Why ant pollination is rare: new evidence and implications of the antibiotic hypothesis. Arthropod Plant Interaction 6:569–661

    Article  Google Scholar 

  • Edwards AM, Auger-Méthé M (2018) Some guidance on using mathematical notation in ecology. Methods Ecol Evol 1:1–10. https://doi.org/10.1111/2041-210x.13105

    Article  Google Scholar 

  • Essenberg CJ (2013) Explaining the Effects of floral density on flower visitor species composition. Am Nat 181:344–356

    Article  PubMed  Google Scholar 

  • Fontaine C, Dajoz I, Meriguet J, Loreau M (2005) Functional diversity of plant-pollinator interaction webs enhances the persistence of plant communities. PLoS Biol 1:1–10. https://doi.org/10.1371/journal.pbio.0040001

    Article  CAS  Google Scholar 

  • García D, Hódar JA, Zamora R, Gómez JM (1996) Experimental study of pollination by ants in Mediterranean high mountain and arid habitats. Oecologia 105:236–242

    Article  PubMed  Google Scholar 

  • Gómez JM (2000) Effectiveness of ants as pollinators of Lobularia maritima: effects on main sequential fitness components of the host plant. Oecologia 122:90–97

    Article  PubMed  Google Scholar 

  • Grant SA, Torvell L, Sim EM, Small JL, Armstrong RH (1996) Controlled grazing studies on nardus grassland: effects of between-tussock sward height and species of grazer on nardus utilization and floristic composition in two fields in scotland. J Appl Ecol 5:1053–1064

    Article  Google Scholar 

  • Hadar L, Noy-Meir I, Perevolotsky A (2009) The effect of shrub clearing and grazing on the composition of a Mediterranean plant community: functional groups versus species. J Veg Sci 10:673–682

    Article  Google Scholar 

  • Heleno R, Devoto M, Pocock M (2012) Connectance of species interaction networks and conservation value: is it any good to be well connected? Ecol Ind 14:7–10

    Article  Google Scholar 

  • Herrera CM, Herrera J, Espalander X (1984) Nectar thievery by ants from southern Spanish insect-pollinated flowers. Insectes Soc 2:142–154

    Article  Google Scholar 

  • Isselstein J, Jeangros B, Pavlu V (2005) Agronomic aspect of biodiversity targeted management of temperate grassland in Europe—a review. Agron Res 3:139–151

    Google Scholar 

  • Junges AH, Bremm C, Fontana DC, Oliveira CAO, Schaparini LP, Carvalho PCF (2016) Temporal profiles of vegetation indices for characterizing grazing intensity on natural grasslands in Pampa biome. Sci Agric 73:332–337

    Article  Google Scholar 

  • Kaiser-Bunbury CN, Blüthgen N (2015) Integrating network ecology with applied conservation: a synthesis and guide to implementation. AoB Plants 1:1–10. https://doi.org/10.1093/aobpla/plv076

    Article  CAS  Google Scholar 

  • Klein AM, Vaissiére BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T (2007) Importance of pollinators in changing landscapes for world crops. Proc Royal Soc B 274:303–313

    Article  Google Scholar 

  • Krishna A, Guimarães PR Jr, Jordano P, Bascompte J (2008) A neutral-niche theory of nestedness in mutualistic networks. Oikos 117:1609–1618

    Article  Google Scholar 

  • Lara-Romero C, García C, Iriondo JM (2015) Direct and indirect effects of shrub encroachment on alpine grasslands mediated by plant-flower-visitor interactions. Funct Ecol 1:1–10. https://doi.org/10.1111/1365-2435.12637

    Article  Google Scholar 

  • Lázaro A, Tscheulin T, Devalez J, Nakas G, Stefanaki A, Hanlidou E, Petanidou T (2016) Moderation is best: effects of grazing intensity on plant–flower visitor networks in Mediterranean communities. Ecol Appl. https://doi.org/10.1890/15-0202.1

    Article  PubMed  Google Scholar 

  • Lupatini M, Jacques RJS, Antoniolli ZI, Suleiman AKA, Fulthorpe RR, Roesch LFW (2013) Land-use change and soil type are drivers of fungal and archaeal communities in the Pampa biome. World J Microbiol Biotechnol 29:223–233

    Article  CAS  PubMed  Google Scholar 

  • Mabry TM, Jones SB, Burnett WC (1977) Evolutionary implications of sesquiterpene lactones in Vernonia (Compositae) and Mammalian Herbivores. Taxon 26:203–207

    Article  Google Scholar 

  • Martín-Gonzáles AM, Dalsgaard B, Nogués-Bravo D, Graham CH et al (2015) The macroecology of phylogenetically structured hummingbird-plant networks. Glob Ecol Biogeogr. https://doi.org/10.1111/geb.12355

    Article  Google Scholar 

  • Mayer C, Soka G, Picker M (2006) The importance of monkey beetle (Scarabaeidae: Hopliini) pollination for Aizoaceae and Asteraceae in grazed and ungrazed areas at Paulshoek, Succulent Karoo, South Africa. J Insect Conserv 10:323–333

    Article  Google Scholar 

  • Memmot J (1999) The structure of a plant-pollinator food web. Ecol Lett 2:276–280

    Article  Google Scholar 

  • Milchunas DG, Sala OE, Laurenroth WK (1988) A Generalized model of the effects of grazing by large herbivores on grassland community structure. Am Nat 132:87–106

    Article  Google Scholar 

  • Moeller DA, Geber M, Eckhart V, Tiffin P (2012) Reduced pollinator service and elevated pollen limitation at the geographic range limit of an annual plant. Ecology 93:1036–1048

    Article  PubMed  Google Scholar 

  • Nabinger C, de Moraes A, Maraschin GE (2000) Campos in Southern Brazil. In: Lemaire G, Hodgson J, Moraes A, Carvalho PC, Nabinger Ceditors (eds). Grassland Ecophysiology and Grazing Ecology. CABI, New York (USA), pp 355–376

  • Nielsen A, Bascompte J (2007) Ecological networks, nestedness and sampling effort. J Ecol 95:1134–1141

    Article  Google Scholar 

  • Nielsen A, Totland Ø (2013) Structural properties of mutualistic networks withstand habitat degradation while species functional roles might change. Oikos 123:323–333

    Article  Google Scholar 

  • Okuyama T, Holland JN (2008) Network structural properties mediate the stability of mutualistic communities. Ecol Lett 11:208–216

    Article  PubMed  Google Scholar 

  • Oleques SS, Overbeck GE, de Avila Jr RS (2017) Flowering phenology and plant-pollinator interactions in a grassland community of Southern Brazil. Flora 229:141–146

    Article  Google Scholar 

  • Olesen JM, Bascompte J, Dupont YL, Jordano P (2007) The modularity of pollination networks. PNAS 104(50):19891–19896

    Article  PubMed  PubMed Central  Google Scholar 

  • Olff H, Ritchie M (1998) Effects of herbivores on grassland plant diversity. Trends Ecol Evol 13:261–265

    Article  CAS  PubMed  Google Scholar 

  • Olito C, Fox JW (2015) Species traits and abundances predict metrics of plant-pollinator network structure, but not pairwise interactions. Oikos 124:428–436

    Article  Google Scholar 

  • Overbeck GE, Muller SC, Pillar VD, Pfandenhauer J (2005) Fine-scale post-fire dynamics in southern Brazilian subtropical grassland. J Veg Sci 16:655–664

    Article  Google Scholar 

  • Overbeck G, Muller SC, Fidelis A, Pfadenhauer J, Pillar DV, Blanco CC, Boldrini II, Both R, Forneck D (2007) Brazil’s neglected biome: the South Brazilian Campos. Perspect Plant Ecol 9:101–116

    Article  Google Scholar 

  • Pillar VD, Focht T (2003) Spatial patterns and relations with site factors in a grassland under grazing. Braz J Biol. https://doi.org/10.1590/s1519-69842003000300008

    Article  PubMed  Google Scholar 

  • Pinheiro M, Abrão BE, Harter-Marques B, Miotto STS (2008) Floral resources used by insects in a grassland community in Southern Brazil. Braz J Bot 1:1–10. https://doi.org/10.1590/s0100-84042008000300011

    Article  Google Scholar 

  • Podgaiski LR, Joner F, Lavorel S, Moretti M, Ibanez S, Mendonça MM Jr, Pillar VD (2013) Spider trait assembly patterns and resilience under fire-induced vegetation change in south brazilian grasslands. PLoS ONE. https://doi.org/10.1371/journal.pone.0060207

    Article  PubMed  PubMed Central  Google Scholar 

  • Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353

    Article  PubMed  Google Scholar 

  • Pykälä J (2004) Cattle grazing increases plant species richness of most species trait groups in mesic semi-natural grasslands. Plant Ecol 175:217–226

    Article  Google Scholar 

  • Rutter SM (2006) Diet preference for grass and legumes in free-ranging domestic sheep and cattle: current theory and future application. Appl Anim Behav Sci 97:17–35

    Article  Google Scholar 

  • Santamaría L, Rodríguez-Gironés MA (2007) Linkage rules for plant-pollinator networks: trait complementarity or exploitation barriers? PLoS Biol 5:e31

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Soares AB, Carvalho PCF, Nabinger C, Semmelmann C, Trindade JK, Guerra E, Freitas TS, Pinto CE, Fontouta-Júnior A, Frizzo A (2005) Produção animal e de forragem em pastagem nativa submetida a distintas ofertas de forragem. Ciência Rural 35:1148–1153

    Article  Google Scholar 

  • Spieman BJ, Inouye BD (2013) Habitat loss alters the architecture of plant—pollinator interaction networks. Ecology 94:2688–2696

    Article  Google Scholar 

  • Thébault E, Fontaine C (2010) Stability of ecological communities and the architecture of mutualistic and trophic networks. Science 329:853–856

    Article  CAS  PubMed  Google Scholar 

  • Torres C, Galleto L (2002) Are nectar-sugar composition and corolla-tube length related to the diversity of insects that visit Asteraceae flowers? Plant Biol 4:360–366

    Article  CAS  Google Scholar 

  • TscharntkeT Tylianakis J (2010) Conserving complexity: global change and community-scale interactions. Biol Conserv 143:2249–2250

    Article  Google Scholar 

  • Tylianakis JM, Tscharntke T, Lewis OT (2007) Habitat modification alters the structure of tropical host-parasitoid food webs. Nature 445:202–205

    Article  CAS  PubMed  Google Scholar 

  • Vanbergen AJ, Woodcock BA, Gray A, Grant F, Telford A, Lambdon P, Chapman DS, Pywell RF, Hear MS, Cavers S (2013) Grazing alters insect visitation networks and plant mating systems. Funct Ecol 28:178–189

    Article  Google Scholar 

  • Vavra M, Parks CG, Wisdom MJ (2007) Biodiversity, exotic plant species, and herbivory: the good, the bad, and the ungulate. For Ecol Manag 246:66–72

    Article  Google Scholar 

  • Vázquez DP, Simberloff D (2004) Indirect effects of an introduced ungulate on pollination and plant reproduction. Ecol Monogr 74:281–308

    Article  Google Scholar 

  • Vázquez DP, Melián CJ, Williams NM, BlüthgenN Krasnov BR, Poulin R (2007) Species abundance and asymmetric interaction strength in ecological networks. Oikos 116:1120–1127

    Article  Google Scholar 

  • Vázquez DP, Blüthgen N, Cagnolo L, Chacoff NP (2009a) Uniting pattern and process in plant-animal mutualistic networks: a review. Ann Bot 103:1445–1457

    Article  PubMed  PubMed Central  Google Scholar 

  • Vázquez DP, Chacoff N, Cagnolo L (2009b) Evaluating multiple determinants of the structure of mutualistic networks. Ecology 90:2039–2046

    Article  PubMed  Google Scholar 

  • Vizentin-Bugoni J, Maruyama PK, Sazima M (2014) Processes entangling interactions in communities: forbidden links are more important than abundance in a hummingbird-plant network. Proc Royal Soc B. https://doi.org/10.1098/rspb.2013.2397

    Article  Google Scholar 

  • Vizentin-Bugoni J, Maruyama PK, Souza CS, Ollerton J, Rech AR, Sazima M (2018) Plant-pollinator networks in the tropics: a review. In: Dáttilo W, Rico-Gray V, Ecological networks in the tropics. Springer, New York

  • Vulliamy B, Potts SG, Willmer PG (2006) The effects of cattle grazing on plant-pollinator communities in a fragmented Mediterranean landscape. Oikos 114:529–543

    Article  Google Scholar 

  • Welti EAR, Joern Anthony (2017) Fire and grazing modulate the structure and resistance of plant–floral visitor networks in a tallgrass prairie. Oecologia. https://doi.org/10.1007/s00442-017-4019-9

    Article  PubMed  Google Scholar 

  • Westerkamp C (1991) Honeybees are poor pollinators—Why? Plant Syst Evol 177:71–75

    Article  Google Scholar 

  • Wolowski M, Cavalheiro LG, Freitas L (2016) Influence of plant–pollinator interactions on the assembly of plant and hummingbird communities. J Ecol. https://doi.org/10.1111/1365-2745.12684

    Article  Google Scholar 

  • Yoshihara Y, Chimeddorj B, Buuveibaatar B, Lhagvasuren B, Takatsukid S (2008) Effects of livestock grazing on pollination on a steppe in eastern Mongolia. Biol Conserv 1419:2376–2386

    Article  Google Scholar 

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Acknowledgements

We thank G. Minervini for field work support, M. Pinheiro (bees), B.R. Garcete-Barret (wasps), J. Duarte (flies), M. Morales (flies-Syrphidae), M.S. Pires (ants), N. Mega (butterflies) and D. Lucas (plants) for their help with species identification and three anonymous reviewers for their valuable comments. We also thank Stephen Tyndel for valuable suggestions on the manuscript and linguistic edits. This work was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) funding [grant number 403750/2012-1], [grant number 477618/2013-8] and in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001. SSO received a Master scholarship from CNPq and GEO a CNPq Grant [310022/2015-0]. JVB thank to U.S. Army Corps of Engineers and the CERL-ERDC (Construction Engineering Research Lab of the Engineer Research & Development Center) for financial support.

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Oleques, S.S., Vizentin-Bugoni, J. & Overbeck, G.E. Influence of grazing intensity on patterns and structuring processes in plant–pollinator networks in a subtropical grassland. Arthropod-Plant Interactions 13, 757–770 (2019). https://doi.org/10.1007/s11829-019-09699-8

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