, Volume 143, Issue 1, pp 126–135 | Cite as

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

  • Alejandro A. Muñoz
  • Constanza Celedon-Neghme
  • Lohengrin A. Cavieres
  • Mary T. K. Arroyo
Plant Animal Interactions


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.


Bottom-up limitation Central Chilean Andes Nutrient addition Plant–pollinator interactions Plant reproductive output 


  1. 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 205–227Google Scholar
  2. Arroyo MTK, Armesto JJ, Villagrán C (1981) Plant phenological patterns in the high Andean Cordillera of central Chile. J Ecol 69:205–223Google Scholar
  3. 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 69:82–97Google Scholar
  4. 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 149:187–203Google Scholar
  5. Atkin OK, Collier DE (1992) Relationship between soil-nitrogen and floristic variation in late snow areas of the Kosciusko alpine region. Aust J Bot 40:139–149Google Scholar
  6. Baskin CC, Baskin JM (1998) Seeds. Ecology, biogeography, and evolution of dormancy and germination. Academic, New YorkGoogle Scholar
  7. Bechtold HA, Forbis TA, Bowman WD, Diggle PK (2002) Lack of reproductive plasticity in alpine Saxifraga rhomboidea (Saxifragaceae). Nordic J Bot 22:361–368Google Scholar
  8. Bierzychudek P (1981) Pollinator limitation of plant reproductive effort. Am Nat 117:838–840CrossRefGoogle Scholar
  9. Billings WD, Mooney HA (1968) The ecology of arctic and alpine plants. Biol Rev 43:481–529Google Scholar
  10. Bingham RA, Orthner AR (1998) Efficient pollination of alpine plants. Nature 391:238–239CrossRefGoogle Scholar
  11. Bosch M, Waser NM (2001) Experimental manipulation of plant density and its effect on pollination and reproduction of two confamilial montane herbs. Oecologia 126:76–83CrossRefGoogle Scholar
  12. Bowman WD, Bilbrough CJ (2001) Influence of a pulsed nitrogen supply on growth and nitrogen uptake in alpine graminoids. Plant Soil 233:283–290CrossRefGoogle Scholar
  13. Bowman WD, Conant RT (1994) Shoot growth dynamics and photosynthetic response to increased nitrogen availability in the alpine willow Salix glauca. Oecologia 97:93–99CrossRefGoogle Scholar
  14. Bowman WD, Theodose TA, Schardt JC, Conant RT (1993) Constraints of nutrient availability on primary production in two alpine tundra communities. Ecology 74:2085–2097Google Scholar
  15. 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 101:217–227CrossRefGoogle Scholar
  16. Brown BJ, Mitchell RJ, Graham SA (2002) Competition for pollination between an invasive species (purple loosestrife) and its native congener. Ecology 83:2328–2336Google Scholar
  17. Burd M (1994) Bateman’s principle and plant reproduction: the role of pollen limitation in fruit and seed set. Bot Rev 60:83–139Google Scholar
  18. Campbell DR, Halama KJ (1993) Resource and pollen limitations to lifetime seed production in a natural plant population. Ecology 74:1043–1051Google Scholar
  19. 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 71:337–347Google Scholar
  20. Cavieres LA, Peñaloza A, Arroyo MK (2000) Altitudinal vegetation belts in the high-Andes of central Chile (33°). Rev Chil Hist Nat 73:331–344Google Scholar
  21. Chapin FS III (1980) The mineral nutrition of wild plants. Annu Rev Ecol Syst 11:233–260CrossRefGoogle Scholar
  22. Chapin FS III, Vitousek PM, Van Cleve K (1986) The nature of nutrient limitation in plant communities. Am Nat 127:48–58CrossRefGoogle Scholar
  23. Dawes-Gromadzki TZ (2002) Trophic trickles rather than cascades: conditional top-down and bottom-up dynamics in an Australian chenopod shrubland. Aust Ecol 27:490–508CrossRefGoogle Scholar
  24. 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 40:804–814CrossRefGoogle Scholar
  25. Dyer LA, Letourneau DK (1999) Relative strengths of top-down and bottom-up forces in a tropical forest community. Oecologia 119:265–274CrossRefGoogle Scholar
  26. Galen C (1985) Regulation of seed set in Polemonium viscosum: floral scents, pollination, and resources. Ecology 66:792–797Google Scholar
  27. Galen C, Zimmer KA, Newport ME (1987) Pollination in floral scent morphs of Polemonium viscosum: a mechanism for disruptive selection on flower size. Evolution 41:599–606Google Scholar
  28. 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 88:256–266CrossRefGoogle Scholar
  29. 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 130:476–483CrossRefGoogle Scholar
  30. Gugerli F (1998) Effect of elevation on sexual reproduction in alpine populations of Saxifraga oppositifolia (Saxifragaceae). Oecologia 114:60–66CrossRefGoogle Scholar
  31. 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 66:389–402Google Scholar
  32. Heer C, Körner C (2002) High elevation pioneer plants are sensitive to mineral nutrient addition. Basic Appl Ecol 3:39–47Google Scholar
  33. Holzmann HP and Haselwandter K (1988) Contribution of nitrogen fixation to nitrogen nutrition in an alpine sedge community (Caricetum curvulae). Oecologia 76:298–302CrossRefGoogle Scholar
  34. 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 73:724–732Google Scholar
  35. 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 102:174–179CrossRefGoogle Scholar
  36. Johnston MO (1991) Natural selection of floral traits in two species of Lobelia with different pollinators. Evolution 45:1468–1479Google Scholar
  37. Jonasson S (1992) Plant responses to fertilization and species removal in tundra related to community structure and clonality. Oikos 63:420–429Google Scholar
  38. Körner C (1989) The nutritional status of plants from high altitudes. Oecologia 81:379–391Google Scholar
  39. Körner C (1999) Alpine plant life. Functional plant ecology of high mountain ecosystems. Springer, Berlin Heidelberg New YorkGoogle Scholar
  40. Larson BMH, Barrett SCH (2000) A comparative analysis of pollen limitation in flowering plants. Biol J Linn Soc 69:503–520CrossRefGoogle Scholar
  41. Lëhtila K, Strauss SY (1997) Leaf damage by herbivores affect attractiveness to pollinators in wild radish Raphanus raphanistrum. Oecologia 111:396–403CrossRefGoogle Scholar
  42. Marschner H (1995) Mineral nutrition of higher plants. Academic, LondonGoogle Scholar
  43. Mattila E, Kuitunen MT (2000) Nutrient versus pollination limitation in Platanthera bifolia and Dactylorhiza incarnata (Orchidaceae). Oikos 89:360–366Google Scholar
  44. 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 41:277–286Google Scholar
  45. 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, SantiagoGoogle Scholar
  46. 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 138:66–73CrossRefPubMedGoogle Scholar
  47. Nagy L, Proctor J (1997) Plant growth and reproduction on a toxic alpine ultramafic soil: adaptation to nutrient limitation. New Phytol 137:267–274CrossRefGoogle Scholar
  48. 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 97:3–17CrossRefGoogle Scholar
  49. Page AL (1983) Methods of soil analysis. Part 2: Chemical and microbiological properties. American Society of Agronomy, MadisonGoogle Scholar
  50. 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 82:307–318Google Scholar
  51. 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 72:61–66Google Scholar
  52. Polis GA, Strong DR (1996) Food web complexity and community dynamics. Am Nat 147:813–846CrossRefGoogle Scholar
  53. 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 86:315–327CrossRefGoogle Scholar
  54. 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, SantiagoGoogle Scholar
  55. Schemske DW, Horvitz CC (1988) Plant–animal interactions and fruit production in a neotropical herb: a path analysis. Ecology 69:1128–1137Google Scholar
  56. Schmitz OJ, Hambäck PA, Beckerman AP (2000) Trophic cascades in terrestrial systems: a review of the effects of carnivore removals on plants. Am Nat 155:141–153CrossRefPubMedGoogle Scholar
  57. 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 33:100–106Google Scholar
  58. Statsoft (1998) Statistica. Version 5.1. Statsoft, USAGoogle Scholar
  59. Stephenson AG (1981) Flower and fruit abortion: proximate causes and ultimate functions. Annu Rev Ecol Syst 12:253–279CrossRefGoogle Scholar
  60. Theodose TA, Bowman WD (1997) Nutrient availability, plant abundance, and species diversity in two alpine tundra communities. Ecology 78:1861–1872Google Scholar
  61. Totland Ø, Sottocornola M (2001) Pollen limitation of the reproductive success in two sympatric alpine willows (Salicaceae) with contrasting pollination strategies. Am J Bot 88:1011–1015PubMedGoogle Scholar
  62. Willson MF, Price PW (1980) Resource limitation of fruit and seed production in some Asclepias species. Can J Bot 58:2229–2233Google Scholar
  63. 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 67:490–502Google Scholar
  64. 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 32:438–448Google Scholar
  65. Zar JH (1996) Biostatistical analysis, 3rd edn. Prentice Hall, New JerseyGoogle Scholar
  66. Zimmerman M, Pyke GH (1988) Reproduction in Polemonium: assessing the factors limiting seed set. Am Nat 131:723–738CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • Alejandro A. Muñoz
    • 1
  • Constanza Celedon-Neghme
    • 1
  • Lohengrin A. Cavieres
    • 1
  • Mary T. K. Arroyo
    • 2
  1. 1.ECOBIOSIS, Departamento de Botánica, Facultad de Ciencias Naturales y OceanográficasUniversidad de ConcepciónCasilla 160-CChile
  2. 2.CMEB, Laboratorio de Sistemática y Ecología Vegetal, Departamento de Ciencias Ecológicas, Facultad de CienciasUniversidad de ChileCasilla 653Chile

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