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Negative correlation between dispersal investment and canopy openness among populations of the ant-dispersed sedge, Carex lanceolata

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Abstract

Flowering plants exhibit a wide variation in the resources they invest in dispersal structures (dispersal investment), but the environmental correlates still remain unclear in many cases. Canopy openness is predicted to be negatively correlated with dispersal investment, because selective pressures on increased dispersal investment, including host-specific natural enemies and the paucity and/or ephemerality of safe sites, will be more prevalent in shady sites. Here, we tested this prediction by firstly examining the correlation between dispersal investment and canopy openness as well as abundance of the representative natural enemy (rusts, Puccinia spp.) through seven populations of an ant-dispersed sedge, Carex lanceolata (Cyperaceae). Secondly we conducted a cafeteria experiment to verify the effect of intraspecific variation in dispersal investment on diaspore preferences of seed dispersing ants. Lastly, a seedling transplant experiment was performed to clarify whether seed dispersal distances by ants are sufficient to reduce infection by the rusts. We found a negative correlation between dispersal investment and canopy openness, thus supporting the prediction. Moreover, there were more signs of rust infection caused by Puccinia spp. on adult plant leaves in more shady sites. The cafeteria experiment showed that a large ant species (Formica japonica) with relatively long seed dispersal distances tended to prefer diaspores with greater dispersal investments, while smaller ant species with shorter dispersal distances preferred diaspores with lower dispersal investments. The seedling transplant experiment revealed that rust severity in sedge offspring was considerably reduced by the typical seed dispersal distance (ca. 4 m) afforded by the large ant species, F. japonica. The increased rust severity at shady sites, combined with the narrow dispersal ranges of rusts, can partially explain the negative correlation of dispersal investment with canopy openness. These results support the importance of canopy openness as a factor underlying the variations in dispersal investment seen among flowering plants.

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References

  • Alexander HM, Price S, Houser R, Finch D, Tourtellot M (2007) Is there reduction in disease and pre-dispersal seed predation at the border of a host plant's range? Field and herbarium studies of Carex blanda. J Ecol 95:446–457

    Google Scholar 

  • Andersen AN (2019) Responses of ant communities to disturbance: five principles for understanding the disturbance dynamics of a globally dominant faunal group. J Anim Ecol 88:350–362

    PubMed  Google Scholar 

  • Augspurger CK (1984) Seedling survival of tropical tree species: interactions of dispersal distance, light-gaps, and pathogens. Ecology 65:1705–1712

    Google Scholar 

  • Augspurger CK, Salk CF (2017) Constraints of cold and shade on the phenology of spring ephemeral herb species. J Ecol 105:246–254

    CAS  Google Scholar 

  • Blake S, Deem SL, Mossimbo E, Maisels F, Walsh P (2009) Forest elephants: tree planters of the Congo. Biotropica 41:459–468

    Google Scholar 

  • Breshears DD (2006) The grassland–forest continuum: trends in ecosystem properties for woody plant mosaics? Front Ecol Environ 4:96–104

    Google Scholar 

  • Brown N, Jennings S, Wheeler P, Nabe-Nielsen J (2000) An improved method for the rapid assessment of forest understorey light environments. J Appl Ecol 37:1044–1053

    Google Scholar 

  • Browne L, Karubian J (2016) Diversity of palm communities at different spatial scales in a recently fragmented tropical landscapes. Bot J Linn Soc 182:451–464

    Google Scholar 

  • Cheptou PO, Carrue O, Rouifed S, Cantarel A (2008) Rapid evolution of seed dispersal in an urban environment in the weed Crepis sancta. Proc Nat Acad Sci USA 105:3796–3799

    CAS  PubMed  Google Scholar 

  • Christian CE (2001) Consequences of a biological invasion reveal the importance of mutualism for plant communities. Nature 413:635–639

    CAS  PubMed  Google Scholar 

  • Comita LS, Uriarte M, Thompson J, Jonckheere I, Canham CD, Zimmerman JK (2009) Abiotic and biotic drivers of seedling survival in a hurricane-impacted tropical forest. J Ecol 97:1346–1359

    Google Scholar 

  • Develey-Rivière M-P, Galiana E (2007) Resistance to pathogens and host developmental stage: a multifaceted relationship within the plant kingdom. New Phytol 175:405–416

    PubMed  Google Scholar 

  • Edwards W (2005) Plant reward seed dispersers in proportion to their effort: the relationship between pulp mass and seed mass in vertebrate dispersed plants. Evol Ecol 20:365–376

    Google Scholar 

  • Edwards W, Dunlop M, Rodgerson L (2006) The evolution of rewards: seed dispersal, seed size and elaiosome size. J Ecol 94:687–694

    Google Scholar 

  • Effiom EO, Nuñez-Iturri G, Smith HG, Ottosson U, Olsson O (2013) Bushmeat hunting changes regeneration of African rainforests. Proc R Soc B 280:20130246

    PubMed  Google Scholar 

  • Encinas-Viso F, Revilla TA, Velzen EV, Etienne RS (2014) Frugivores and cheap fruits make fruiting fruitful. J Evol Biol 27:313–324

    CAS  PubMed  Google Scholar 

  • Ezoe H (1998) Optimal dispersal range and seed size in a stable environment. J Theor Biol 190:287–293

    CAS  PubMed  Google Scholar 

  • Farber DH, Mundt CC (2017) Effect of plant age and leaf position on susceptibility to wheat stripe rust. Phytopathology 107:412–417

    CAS  PubMed  Google Scholar 

  • Farber DH, Medlock J, Mundt CC (2017) Local dispersal of Puccinia striiformis f. sp. tritici from isolated source lesions. Plant Pathol 66:28–37

    CAS  PubMed  Google Scholar 

  • Fragoso JM, Silvius KM, Correa JA (2003) Long-distance seed dispersal increased seed survival and aggregates tropical trees. Ecology 84:1998–2006

    Google Scholar 

  • Frezal L, Robert C, Bancal M-O, Lannou C (2009) Local dispersal of Puccinia triticina and wheat canopy structure. Phytopathology 99:1216–1224

    PubMed  Google Scholar 

  • Galetti M, Guevara R, Côrtes MC, Fadini R, Matter SV, Leite AB, Labecca F, Ribeiro T, Carvalho CS, Collevatti RG, Pires MM, Guimarães PR Jr, Brancalion PH, Ribeiro MC, Jordano P (2013) Functional extinction of birds drives rapid evolutionary changes in seed size. Science 340:1086–1090

    CAS  PubMed  Google Scholar 

  • Godoy O, Saldaña A, Fuentes N, Valladares F, Gianoli E (2011) Forests are not immune to plant invasions: phenotypic plasticity and local adaptation allow Prunella vugaris to colonize a temperate evergreen rainforest. Biol Invasions 13:1615–1625

    Google Scholar 

  • Gotsch SG, Powers JS, Lerdau MT (2010) Leaf traits and water relations of 12 evergreen species in Costa Rican wet and dry forests: patterns of intra-specific variation across forests and seasons. Plant Ecol 211:133–146

    Google Scholar 

  • Goulart MF, Lovato MB, Barros FV, Valladares F, Lemos-Filho JP (2011) Which extent is plasticity to light involved in the ecotypic differentiation of a tree species from savanna and forest? Biotropica 43:695–703

    Google Scholar 

  • Green DS (1983) The efficacy of dispersal in relation to safe site density. Oecologia 56:356–358

    PubMed  Google Scholar 

  • Hanzawa FM, Beattie AJ, Culver DC (1988) Directed dispersal: demographic analysis of an ant-seed mutualism. Am Nat 131:1–13

    Google Scholar 

  • Hashimoto Y, Ishimaru K, Kuroda A, Masunaga S, Yokota J (2012) Effects of mowing resumption on recovery and richness of grassland plant species in abondoned grasslands dominated by dwarf bamboo. Landsc Kenkyu 5:69–76

    Google Scholar 

  • Howe HF, Smallwood J (1982) Ecology of seed dispersal. Ann Rev Ecol Syst 13:201–228

    Google Scholar 

  • Howe HF, Schupp EW, Westley LC (1985) Early consequences of seed dispersal for a neotropical tree (Virola surinamensis). Ecology 66:781–791

    Google Scholar 

  • Hughes L, Westoby M (1992) Effect of diaspore characteristics on removal of seeds adapted for dispersal by ants. Ecology 73:1300–1312

    Google Scholar 

  • Iwata K, Eguchi K, Yamane S (2005) A case study on urban ant fauna of southern kyushu, Japan, with notes on a new monitoring protocol (Insecta, Hymenoptera, Formicidae). J Asia Pac Entomol 8:263–272

    Google Scholar 

  • Koyanagi T, Kusumoto Y, Yamamoto S, Okubo S, Takeuchi K (2009) Historical impacts on linear habitats: the present distribution of grassland species in forest-edge vegetation. Biol Conserv 142:1674–1684

    Google Scholar 

  • Kwon T-S, Lee CM, Sung JH (2014) Diversity decrease of ant (Formicidae, Hymenoptera) after a forest disturbance: different responses among functional guilds. Zool Stud 53:37

    Google Scholar 

  • Leal LC, Neto MCL, de Oliveira AFM, Andersen AN, Leal IR (2014) Myrmecochores can target high-quality disperser ants: variation in elaiosome traits and ant preferences for myrmecochores Euphorbiaceae in Brazilian Caatinga. Oecologia 174:493–500

    PubMed  Google Scholar 

  • Leal IR, Leal LC, Andersen AN (2015) The benefits of myrmecochory: a matter of stature. Biotropica 47:281–285

    Google Scholar 

  • Lopez-Gallego C, O'Neil P (2014) Genetic variation and the potential response to selection on leaf traits after habitat degradation in a long-lived cycad. Evol Ecol 28:775–791

    Google Scholar 

  • Manzaneda AJ, Rey PJ (2012) Geographical and interspecific variation and the nutrient-enrichment hypothesis as an adaptive advantage of myrmecochory. Ecography 35:322–332

    Google Scholar 

  • Manzaneda AJ, Fedriani JM, Rey PJ (2005) Adaptive advantages of myrmecohcory: the predator-avoidance hypothesis tested over a wide geographic range. Ecography 28:583–592

    Google Scholar 

  • Mark S, Olesen JM (1996) Importance of elaiosome size to removal of ant-dispersed seeds. Oecologia 107:95–101

    PubMed  Google Scholar 

  • Martens SN, Breshears DD, Meyer CW (2000) Spatial distributions of understory light along the grassland/forest continuum: effects of cover, height, and spatial pattern of tree canopies. Ecol Model 126:79–93

    Google Scholar 

  • Meekins JF, McCarthy BC (2000) Responses of the biennial forest herb Alliaria petiolata to variation in population density, nutrient addition and light availability. J Ecol 88:447–463

    Google Scholar 

  • Muller-Landau HC, Levin SA, Keymer JE (2003) Theoretical perspectives on evolution of long-distance dispersal and the example of specialized pests. Ecology 84:1957–1967

    Google Scholar 

  • Norghauer JM, Malcolm JR, Zimmerman BL (2008) Canopy cover mediates interactions between a specialist caterpillar and seedlings of a neotropical tree. J Ecol 96:103–113

    Google Scholar 

  • O'Dowd DJ, Hay ME (1980) Mutualism between harvester ants and a desert ephemeral: seed escape from rodents. Ecology 61:531–540

    Google Scholar 

  • Packer A, Clay K (2000) Soil pathogens and spatial patterns of seedling mortality in a temperate tree. Nature 404:278–281

    CAS  PubMed  Google Scholar 

  • Packer A, Clay K (2003) Soil pathogens and Prunus serotina seedling and sapling growth near conspecific trees. Ecology 84:108–119

    Google Scholar 

  • Paul ND, Ayres PG (1987) Water stress modifies intraspecific interference between rust (Puccinia lagenophorae Cooke)-infected and healthy groudsel (Senecio vulgaris L.). New Phytol 106:555–566

    Google Scholar 

  • Pigot AL, Leather SR (2008) Invertebrate predators drive distance-dependent patterns of seedling mortality in a temperate tree Acer pseudoplatanus. Oikos 117:521–530

    Google Scholar 

  • R Foundation for Statistical Computing (2018) R: a language and environment for statistical computing. Version 3.5.1. R Foundation for Statistical Computing, Vienna, Austria

  • Reich PB, Tjoelker MG, Walters MB, Vanderklein DW, Buschena C (1998) Close association of RGR, leaf and root morphology, seed mass and shade tolerance in seedlings of nine boreal tree species grown in high and low light. Funct Ecol 12:327–338

    Google Scholar 

  • Robert C, Bancal M-O, Ney B, Lannou C (2005) Wheat leaf photosynthesis loss due to leaf rust, with respect to lesion development and leaf nitrogen status. New Phytol 165:227–241

    PubMed  Google Scholar 

  • Roberts MR, Paul ND (2006) Seduced by the dark side: integrating molecular and ecological perspectives on the influence of light on plant defence against pests and pathogens. New Phytol 170:677–699

    CAS  PubMed  Google Scholar 

  • Sack L, Scoffoni C (2013) Leaf venation: structure, function, development, evolution, ecology and applications in the past, present and future. New Phytol 198:983–1000

    PubMed  Google Scholar 

  • Sendall KM, Lusk CH, Reich PB (2016) Trade-offs in juvenile growth potential vs. shade tolerance among subtropical rain forest trees on soils of contrasting fertility. Funct Ecol 30:845–855

    Google Scholar 

  • Springer YP (2002) Edaphic quality and plant-pathogen interactions: effects of soil calcium on fungal infection of a serpentine flax. Ecology 90:1852–1862

    Google Scholar 

  • Sultan SE (2001) Phenotypic plasticity for fitness components in Polygonum species of contrasting ecological breadth. Ecology 82:328–343

    Google Scholar 

  • Takeuchi Y, Kenta T, Nakashizuka T (2005) Comparison of sapling demography of four dipterocarp species with different seed-dispersal strategies. For Ecol Manag 1–3:237–248

    Google Scholar 

  • Tanaka K, Tokuda M (2016) Seed dispersal distances by ant partners reflect preferential recruitment patterns in two ant-dispersed sedges. Evol Ecol 30:943–952

    Google Scholar 

  • Terborgh J, Nuñez-Iturri G, Pitman NCA, Valverde FHC, Alvarez P, Swamy V, Pringle EG, Paine CET (2008) Tree recruitment in an empty forest. Ecology 89:1757–1768

    PubMed  Google Scholar 

  • Thomson FJ, Letten AD, Tamme R, Edwards W, Moles AT (2018) Can dispersal investment explain why tall plant species achieve longer dispersal distances than short plant species? New Phytol 217:407–415

    PubMed  Google Scholar 

  • Tinya F, Márialigeti S, Király I, Németh B, Ódor P (2009) The effect of light conditions on herbs, bryophytes and seedlings of temperate mixed forests in Őrség, western Hungary. Plant Ecol 204:69–81

    Google Scholar 

  • Venable DL, Dyreson E, Pinero D, Becerra JX (1998) Seed morphometrics and adaptive geographic differentiation. Evolution 52:344–354

    PubMed  Google Scholar 

  • von Wettberg EJ, Huber H, Schmitt J (2005) Interacting effects of microsite quality, plasticity and dispersal distance from the parental site on fitness in a natural population of Impatiens capensis. Evol Ecol Res 7:531–548

    Google Scholar 

  • Washitani I, Tang Y (1991) Microsite variation in light availability and seedling growth of Quercus serrata in a temperate pine forest. Ecol Res 6:305–316

    Google Scholar 

  • Wenny DG, Levey DJ (1998) Directed seed dispersal by bellbirds in a tropical cloud forest. Proc Nat Acad Sci USA 95:6204–6207

    CAS  PubMed  Google Scholar 

  • Westerband AC, Horvitz CC (2015) Interactions between plant size and canopy openness influence vital rates and life-history tradeoffs in two neotropical understory herbs. Am J Bot 102:1290–1299

    CAS  PubMed  Google Scholar 

  • Whigham DF (2004) Ecology of woodland herbs in temperate deciduous forests. Ann Rev Ecol Evol Syst 35:583–621

    Google Scholar 

  • Wright IJ, Westoby M, Reich PB (2002) Convergence towards higher leaf mass per area in dry and nutrient-poor habitats has different consequences for leaf life span. J Ecol 90:534–543

    Google Scholar 

  • Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas M-L, Niinemets Ü, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R (2008) The worldwide leaf economics spectrum. Nature 428:822–827

    Google Scholar 

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Acknowledgements

We thank Y. Yamaoka for identifying the rusts found on C. lanceolata as Puccinia spp. We sincerely appreciate M. Tanaka for consistent help with the fieldwork.

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  1. Faculty of Agriculture, Saga University, Saga, Japan

    Koki Tanaka & Makoto Tokuda

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  1. Koki Tanaka
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Correspondence to Koki Tanaka.

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Communicated by E.T.F Witkowski.

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Tanaka, K., Tokuda, M. Negative correlation between dispersal investment and canopy openness among populations of the ant-dispersed sedge, Carex lanceolata. Plant Ecol 221, 1105–1115 (2020). https://doi.org/10.1007/s11258-020-01065-6

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