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Bottom-up effects of nutrient availability on flower production, pollinator visitation, and seed output in a high-Andean shrub

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Abstract

Soil nutrient availability directly enhances vegetative growth, flowering, and fruiting in alpine ecosystems. However, the impacts of nutrient addition on pollinator visitation, which could affect seed output indirectly, are unknown. In a nutrient addition experiment, we tested the hypothesis that seed output in the insect-pollinated, self-incompatible shrub, Chuquiraga oppositifolia (Asteraceae) of the Andes of central Chile, is enhanced by soil nitrogen (N) availability. We aimed to monitor total shrub floral display, size of flower heads (capitula), pollinator visitation patterns, and seed output during three growing seasons on control and N addition shrubs. N addition did not augment floral display, size of capitula, pollinator visitation, or seed output during the first growing season. Seed mass and viability were 25–40% lower in fertilised shrubs. During the second growing season only 33% of the N addition shrubs flowered compared to 71% of controls, and a significant (50%) enhancement in vegetative growth occurred in fertilised shrubs. During the third growing season, floral display in N addition shrubs was more than double that of controls, received more than twice the number of insect pollinator visits, and seed output was three- to four-fold higher compared to controls. A significant (50%) enhancement in vegetative growth again occurred in N addition shrubs. Results of this study strongly suggest that soil N availability produces strong positive bottom-up effects on the reproductive output of the alpine shrub C. oppositifolia. Despite taking considerably longer to be manifest in comparison to the previously reported top-down indirect negative effects of lizard predators in the same study system, our results suggest that both bottom-up and top-down forces are important in controlling the reproductive output of an alpine shrub.

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References

  • Arroyo MTK, Squeo FA (1990) Relationship between plant breeding systems and pollination. In: Kawano S (ed) Biological approaches and evolutionary trends in plants. Academic, New York, pp 205–227

    Google Scholar 

  • Arroyo MTK, Armesto JJ, Villagrán C (1981) Plant phenological patterns in the high Andean Cordillera of central Chile. J Ecol 69:205–223

    Google Scholar 

  • Arroyo MTK, Primack R, Armesto J (1982) Community studies in pollination ecology in the high temperate Andes of central Chile. I. Pollination mechanisms and altitudinal variation. Am J Bot 69:82–97

    Google Scholar 

  • Arroyo MTK, Armesto JJ, Primack RB (1985) Community studies in pollination ecology in the high temperate Andes of central Chile. II. Effect of temperature on visitation rates and pollination possibilities. Plant Syst Evol 149:187–203

    Google Scholar 

  • Atkin OK, Collier DE (1992) Relationship between soil-nitrogen and floristic variation in late snow areas of the Kosciusko alpine region. Aust J Bot 40:139–149

    CAS  Google Scholar 

  • Baskin CC, Baskin JM (1998) Seeds. Ecology, biogeography, and evolution of dormancy and germination. Academic, New York

    Google Scholar 

  • Bechtold HA, Forbis TA, Bowman WD, Diggle PK (2002) Lack of reproductive plasticity in alpine Saxifraga rhomboidea (Saxifragaceae). Nordic J Bot 22:361–368

    Google Scholar 

  • Bierzychudek P (1981) Pollinator limitation of plant reproductive effort. Am Nat 117:838–840

    Article  Google Scholar 

  • Billings WD, Mooney HA (1968) The ecology of arctic and alpine plants. Biol Rev 43:481–529

    Google Scholar 

  • Bingham RA, Orthner AR (1998) Efficient pollination of alpine plants. Nature 391:238–239

    Article  Google Scholar 

  • Bosch M, Waser NM (2001) Experimental manipulation of plant density and its effect on pollination and reproduction of two confamilial montane herbs. Oecologia 126:76–83

    Article  Google Scholar 

  • Bowman WD, Bilbrough CJ (2001) Influence of a pulsed nitrogen supply on growth and nitrogen uptake in alpine graminoids. Plant Soil 233:283–290

    Article  CAS  Google Scholar 

  • Bowman WD, Conant RT (1994) Shoot growth dynamics and photosynthetic response to increased nitrogen availability in the alpine willow Salix glauca. Oecologia 97:93–99

    Article  Google Scholar 

  • Bowman WD, Theodose TA, Schardt JC, Conant RT (1993) Constraints of nutrient availability on primary production in two alpine tundra communities. Ecology 74:2085–2097

    Google Scholar 

  • Bowman WD, Theodose TA, Fisk MC (1995) Physiological and production responses of plant growth forms to increases in limiting resources in alpine tundra: implications for differential community response to environmental change. Oecologia 101:217–227

    Article  Google Scholar 

  • Brown BJ, Mitchell RJ, Graham SA (2002) Competition for pollination between an invasive species (purple loosestrife) and its native congener. Ecology 83:2328–2336

    Google Scholar 

  • Burd M (1994) Bateman’s principle and plant reproduction: the role of pollen limitation in fruit and seed set. Bot Rev 60:83–139

    Google Scholar 

  • Campbell DR, Halama KJ (1993) Resource and pollen limitations to lifetime seed production in a natural plant population. Ecology 74:1043–1051

    Google Scholar 

  • Cavieres LA, Peñaloza A, Papic C, Tambutti M (1998) Efecto nodriza de Laretia acaulis en plantas de la zona andina de Chile central. Rev Chil Hist Nat 71:337–347

    Google Scholar 

  • Cavieres LA, Peñaloza A, Arroyo MK (2000) Altitudinal vegetation belts in the high-Andes of central Chile (33°). Rev Chil Hist Nat 73:331–344

    Google Scholar 

  • Chapin FS III (1980) The mineral nutrition of wild plants. Annu Rev Ecol Syst 11:233–260

    Article  Google Scholar 

  • Chapin FS III, Vitousek PM, Van Cleve K (1986) The nature of nutrient limitation in plant communities. Am Nat 127:48–58

    Article  Google Scholar 

  • Dawes-Gromadzki TZ (2002) Trophic trickles rather than cascades: conditional top-down and bottom-up dynamics in an Australian chenopod shrubland. Aust Ecol 27:490–508

    Article  Google Scholar 

  • Dorland E, Robbink R, Messelink JH, Verhoeven JTA (2003) Soil ammonium accumulation after sod cutting hampers the restoration of degraded wet heathlands. J Appl Ecol 40:804–814

    Article  CAS  Google Scholar 

  • Dyer LA, Letourneau DK (1999) Relative strengths of top-down and bottom-up forces in a tropical forest community. Oecologia 119:265–274

    Article  Google Scholar 

  • Galen C (1985) Regulation of seed set in Polemonium viscosum: floral scents, pollination, and resources. Ecology 66:792–797

    Google Scholar 

  • Galen C, Zimmer KA, Newport ME (1987) Pollination in floral scent morphs of Polemonium viscosum: a mechanism for disruptive selection on flower size. Evolution 41:599–606

    Google Scholar 

  • Gerdol R, Brancaleoni L, Menghini M, Marchesini R (2000) Response of dwarf shrubs to neighbour removal and nutrient addition and their influence on community structure in a subalpine heath. J Ecol 88:256–266

    Article  Google Scholar 

  • Gerdol R, Brancaleoni L, Marchesini R, Bragazzi L (2002) Nutrient and carbon relations in subalpine dwarf shrubs after neighbour removal or fertilization in northern Italy. Oecologia 130:476–483

    Article  Google Scholar 

  • Gugerli F (1998) Effect of elevation on sexual reproduction in alpine populations of Saxifraga oppositifolia (Saxifragaceae). Oecologia 114:60–66

    Article  Google Scholar 

  • Havström M, Callaghan TV, Jonasson S (1993) Differential growth responses of Cassiope tetragona, an arctic dwarf-shrub, to environmental perturbations among three contrasting high- and subarctic sites. Oikos 66:389–402

    Google Scholar 

  • Heer C, Körner C (2002) High elevation pioneer plants are sensitive to mineral nutrient addition. Basic Appl Ecol 3:39–47

    Google Scholar 

  • Holzmann HP and Haselwandter K (1988) Contribution of nitrogen fixation to nitrogen nutrition in an alpine sedge community (Caricetum curvulae). Oecologia 76:298–302

    Article  Google Scholar 

  • Hunter MD, Price PW (1992) Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology 73:724–732

    Google Scholar 

  • Johnson SG, Delph LF, Elderkin CL (1995) The effect of petal size manipulations on pollen removal, seed set, and insect-visitor behavior in Campanula america. Oecologia 102:174–179

    Article  Google Scholar 

  • Johnston MO (1991) Natural selection of floral traits in two species of Lobelia with different pollinators. Evolution 45:1468–1479

    Google Scholar 

  • Jonasson S (1992) Plant responses to fertilization and species removal in tundra related to community structure and clonality. Oikos 63:420–429

    Google Scholar 

  • Körner C (1989) The nutritional status of plants from high altitudes. Oecologia 81:379–391

    Google Scholar 

  • Körner C (1999) Alpine plant life. Functional plant ecology of high mountain ecosystems. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Larson BMH, Barrett SCH (2000) A comparative analysis of pollen limitation in flowering plants. Biol J Linn Soc 69:503–520

    Article  Google Scholar 

  • Lëhtila K, Strauss SY (1997) Leaf damage by herbivores affect attractiveness to pollinators in wild radish Raphanus raphanistrum. Oecologia 111:396–403

    Article  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants. Academic, London

    Google Scholar 

  • Mattila E, Kuitunen MT (2000) Nutrient versus pollination limitation in Platanthera bifolia and Dactylorhiza incarnata (Orchidaceae). Oikos 89:360–366

    Google Scholar 

  • Montgomery BR, Kelly D, Robertson AW, Ladley JJ (2003) Pollinator behaviour, not increased resources, boosts seed set on forest edges in a New Zealand Loranthaceous mistletoe. N Z J Bot 41:277–286

    Google Scholar 

  • Muñoz AA (2003) Evaluación experimental de la importancia de efectos indirectos descendentes y ascendentes sobre el éxito reproductivo de Chuquiraga oppositifolia (Asteraceae) en la Cordillera de Los Andes en Chile central. Ph.D. dissertation, Facultad de Ciencias, Universidad de Chile, Santiago

  • Muñoz AA, Arroyo MTK (2004) Negative impacts of a vertebrate predator on insect pollinator visitation and seed output in Chuquiraga oppositifolia, a high Andean shrub. Oecologia 138:66–73

    Article  PubMed  Google Scholar 

  • Nagy L, Proctor J (1997) Plant growth and reproduction on a toxic alpine ultramafic soil: adaptation to nutrient limitation. New Phytol 137:267–274

    Article  CAS  Google Scholar 

  • Nilsson MC, Wardle DA, Zackrisson O, Jäderlund A (2002) Effects of alleviation of ecological stresses on an alpine tundra community over an eight-year period. Oikos 97:3–17

    Article  Google Scholar 

  • Page AL (1983) Methods of soil analysis. Part 2: Chemical and microbiological properties. American Society of Agronomy, Madison

    Google Scholar 

  • Parsons AN, Welker JM, Wookey PA, Press MC, Callaghan TV, Lee JA (1994) Growth responses of four sub-Arctic dwarf shrubs to simulated environmental change. J Ecol 82:307–318

    Google Scholar 

  • Parsons AN, Press MC, Wookey PA, Robinson CH, Callaghan TV, Lee JA (1995) Growth responses of Calamagrostis lapponica to simulated environmental change in the Sub-arctic. Oikos 72:61–66

    Google Scholar 

  • Polis GA, Strong DR (1996) Food web complexity and community dynamics. Am Nat 147:813–846

    Article  Google Scholar 

  • Press MC, Potter JA, Burke MJW, Callaghan TV, Lee JA (1998) Responses of a subarctic dwarf shrub heath community to simulated environmental change. J Ecol 86:315–327

    Article  Google Scholar 

  • Rozzi R (1990) Períodos de floración y especies de polinizadores en poblaciones de Anarthrophyllum cumingii y Chuquiraga oppositifolia que crecen sobre laderas de exposición norte y sur. Masters thesis, Facultad de Ciencias, Universidad de Chile, Santiago

  • Schemske DW, Horvitz CC (1988) Plant–animal interactions and fruit production in a neotropical herb: a path analysis. Ecology 69:1128–1137

    Google Scholar 

  • Schmitz OJ, Hambäck PA, Beckerman AP (2000) Trophic cascades in terrestrial systems: a review of the effects of carnivore removals on plants. Am Nat 155:141–153

    Article  PubMed  Google Scholar 

  • Seastedt TR, Vaccaro L (2001) Plant species richness, productivity, and nitrogen and phosphorus limitations across a snowpack gradient in alpine tundra, Colorado, USA. Arct Antarct Alp Res 33:100–106

    Google Scholar 

  • Statsoft (1998) Statistica. Version 5.1. Statsoft, USA

    Google Scholar 

  • Stephenson AG (1981) Flower and fruit abortion: proximate causes and ultimate functions. Annu Rev Ecol Syst 12:253–279

    Article  Google Scholar 

  • Theodose TA, Bowman WD (1997) Nutrient availability, plant abundance, and species diversity in two alpine tundra communities. Ecology 78:1861–1872

    Google Scholar 

  • Totland Ø, Sottocornola M (2001) Pollen limitation of the reproductive success in two sympatric alpine willows (Salicaceae) with contrasting pollination strategies. Am J Bot 88:1011–1015

    PubMed  Google Scholar 

  • Willson MF, Price PW (1980) Resource limitation of fruit and seed production in some Asclepias species. Can J Bot 58:2229–2233

    Google Scholar 

  • Wookey PA, Parsons AN, Welker JM, Potter JA, Callaghan TV, Lee JA, Press MC (1993) Comparative responses of phenology and reproductive development to simulated environmental change in sub-arctic and high arctic plants. Oikos 67:490–502

    Google Scholar 

  • Wyka T, Galen C (2000) Current and future costs of reproduction in Oxytropis sericea, a perennial plant from the Colorado Rocky Mountains, USA. Arct Antarct Alp Res 32:438–448

    Google Scholar 

  • Zar JH (1996) Biostatistical analysis, 3rd edn. Prentice Hall, New Jersey

    Google Scholar 

  • Zimmerman M, Pyke GH (1988) Reproduction in Polemonium: assessing the factors limiting seed set. Am Nat 131:723–738

    Article  Google Scholar 

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Acknowledgements

We thank N. Binfa, P. Chacón, M. Correa, L. Díaz, S. Henríquez, K. Maldonado, B. Muñoz, A. Rivera, and L. Sotomayor for help in the field. Research benefited from discussions with J.J. Armesto, R.O. Bustamante, F.M. Jaksic, C.G. Jones, and M.F. Willson. R.O. Bustamante and two anonymous reviewers made highly valuable comments on earlier versions of the manuscript. R. Leatherbee is acknowledged for permission to conduct work on El Colorado Ski Complex (ANDACOR S.A) property. Research was supported by FONDECYT 2010032 doctoral research grant to A.A.M, Chilean Millennium Scientific Initiative grants P99-103-F-ICM and P02-051-F ICM to M.T.K.A., and FONDECYT 1030821 research grant to L.A.C. A.A.M is currently a Postdoctoral fellow at Universidad de Concepción, Chile, supported through Mecesup grant UCO9906.

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Correspondence to Alejandro A. Muñoz.

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Muñoz, A.A., Celedon-Neghme, C., Cavieres, L.A. et al. Bottom-up effects of nutrient availability on flower production, pollinator visitation, and seed output in a high-Andean shrub. Oecologia 143, 126–135 (2005). https://doi.org/10.1007/s00442-004-1780-3

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