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Experimental evidence that ptarmigan regulate willow bud production to their own advantage

  • Plant-microbe-animal interactions - Original research
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Abstract

In some ecosystems, vertebrate herbivores increase the nutritional quality and biomass of their food source through repeated grazing, thereby manipulating their environment to support higher densities of animals. We tested whether ptarmigan (Lagopus lagopus and L. muta) are capable of regulating the nutritional quality, abundance, and availability of feltleaf willow (Salix alaxensis) buds using a simulated browsing experiment and a feeding preference study with wild birds. Simulated ptarmigan browsing resulted in smaller buds, but greater numbers of buds per shoot. Furthermore, browsing altered the morphology of willow branches such that buds were at higher densities and closer to snow level compared to unbrowsed controls. Browsing increased the number of willows with accessible buds (buds within 50 cm of snow level) from 55 to 89 %, and increased total accessible bud biomass from 113 ± 30 to 129 ± 50 mg/ramet. Browsing did not affect bud nitrogen or carbon concentration and slightly reduced protein precipitation capacity (tannins) in buds the following winter, indicating that ptarmigan browsing does not induce a defensive response in this species. When branches of broomed (previously browsed) and unbroomed willows were placed in the snow at equal heights, ptarmigan showed no preference for either type; however, they obtained more buds from broomed willows. Increased accessibility and density of willow buds caused by browsing has the potential to increase habitat carrying capacity, thereby supporting higher densities of ptarmigan.

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References

  • Agrawal A, Fishbein M (2006) Plant defense syndromes. Ecology 87:S132–S149

    Article  PubMed  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2013) lme4: Linear mixed-effects models using Eigen and S4. R package version 1:0–5

  • Bergstrom R, Danell K (1987) Effects of simulated winter browsing by moose on morphology and biomass of two birch species. J Ecol 75:533–544

    Article  Google Scholar 

  • Brøseth H, Tufto J, Pederson HC, Steen H, Kastdalen L (2005) Dispersal patterns in a harvested willow ptarmigan population. J Appl Ecol 42:453–459

    Article  Google Scholar 

  • Bryant JP (1987) Feltleaf willow-snowshoe hare interactions: plant carbon/nutrient balance and floodplain succession. Ecology 68:1319–1327

    Article  Google Scholar 

  • Bryant JP (2003) Winter browsing on Alaska feltleaf willow twigs improves leaf nutritional value for snowshoe hares in summer. Oikos 1:25–32

    Article  Google Scholar 

  • Bryant JP, Chapin FS, Klein DR (1983) Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40:357–368

    Article  CAS  Google Scholar 

  • Bryant JP, Wieland GD, Clausen T, Kuropat P (1985) Interactions of snowshoe hare and feltleaf willow in alaska. Ecology 66:1564–1573

    Article  Google Scholar 

  • Budde KB, Gallo L, Marchelli P et al (2011) Wide spread invasion without sexual reproduction? A case study on European willows in Patagonia, Argentina. Biol Invasions 13:45–54. doi:10.1007/s10530-010-9785-9

    Article  Google Scholar 

  • Carroll AL, Quiring DT (2003) Herbivory modifies conifer phenology: induced amelioration by a specialist folivore. Oecologia 136:88–95. doi:10.1007/s00442-003-1240-5

    Article  PubMed  Google Scholar 

  • Christie K, Ruess R, Lindberg MS, Mulder C (2014a) Herbivores influence the growth, reproduction, and morphology of a widespread Arctic willow. PLoS ONE 9:e101716. doi:10.1371/journal.pone.0101716

    Article  PubMed Central  PubMed  Google Scholar 

  • Christie KS, Lindberg MS, Ruess RW, Schmutz JA (2014b) Spatio-temporal patterns of ptarmigan occupancy relative to shrub cover in the Arctic. Polar Biol. doi:10.1007/s00300-014-1504-z

    Google Scholar 

  • Coley PD, Bryant JP, Chapin FS (1985) Resource availability and plant antiherbivore defense. Science 230:895–899

    Article  CAS  PubMed  Google Scholar 

  • Collet D (2004) Willows of interior Alaska. US Fish and Wildlife Service, Fairbanks

    Google Scholar 

  • Craig TP (2010) The resource regulation hypothesis and positive feedback loops in plant–herbivore interactions. Popul Ecol 52:461–473. doi:10.1007/s10144-010-0210-0

    Article  Google Scholar 

  • Craig TP, Price P, Itami J (1986) Resource regulation by a stem-galling sawfly on the arroyo willow. Ecology 67:419–425

    Article  Google Scholar 

  • Danell K, Huss-Danell K (1985) Terrestrial plant tolerance to herbivory. Oikos 44:75–81

    Article  Google Scholar 

  • Danell K, Bergström R, Edenius L (1994) Effects of large mammalian browsers on architecture, biomass, and nutrients of woody plants. J Mamm 75:833–844

    Article  Google Scholar 

  • DeGabriel JL, Wallis IR, Moore BD, Foley WJ (2008) A simple, integrative assay to quantify nutritional quality of browses for herbivores. Oecologia 156:107–116

    Article  PubMed  Google Scholar 

  • Fornara DA, Du Toit JT (2007) Browsing lawns? Responses of Acacia nigrescens to ungulate browsing in an African savanna. Ecology 88:200–209

    Article  CAS  PubMed  Google Scholar 

  • Fox JF, Bryant JP (1984) Instability of the snowshoe hare and woody plant interaction. Oecologia 63:128–135

    Article  Google Scholar 

  • Hakkarainen H, Virtanen R, Honkanen JO, Roininen H (2006) Willow bud and shoot foraging by ptarmigan in relation to snow level in NW Finnish Lapland. Polar Biol 30:619–624. doi:10.1007/s00300-006-0221-7

    Article  Google Scholar 

  • Harrison KA, Bardgett RD (2008) Impacts of grazing and browsing by large herbivores on soils and soil biological properties. In: Gordon IJ, Prins HHT (eds) The ecology of browsing and grazing. Ecological studies, vol 195. Springer, Berlin, pp 201–216

  • Hik ADS, Jefferies RL (1990) Increases in the net above-ground primary production of a salt-marsh forage grass : a test of the predictions of the herbivore-optimization model. J Ecol 78:180–195

    Article  Google Scholar 

  • Hilbert ADW, Swift DM, Detling JK, Dyer MI (1981) Relative growth rates and the grazing optimization hypothesis. Oecologia 51:14–18

    Article  Google Scholar 

  • Hobbs NT (1996) Modification of ecosystems by ungulatates. J Wildl Manag 60:695–713

    Article  Google Scholar 

  • Irving L, West C, Peyton LJ, Paneak S (1966) Migration of willow ptarmigan in arctic Alaska. Arctic 20:77–85

    Google Scholar 

  • Klimesová J, Klimeš L (2007) Bud banks and their role in vegetative regeneration—a literature review and proposal for simple classification and assessment. Perspect Plant Ecol Evol Syst 8:115–129. doi:10.1016/j.ppees.2006.10.002

    Article  Google Scholar 

  • Kuznetsova A, Brockhoff PB, Haubo R, Christensen B (2014) lmer Test: tests for random and fixed effects for linear mixed effect models (lmer objects of lme4 package). R package version 2:0–6

  • Makhabu SW, Skarpe C, Hytteborn H (2006) Elephant impact on shoot distribution on trees and on rebrowsing by smaller browsers. Acta Oecol 30:136–146. doi:10.1016/j.actao.2006.02.005

    Article  Google Scholar 

  • Martin JS, Martin MM (1982) Tannin assays in ecological studies: lack of correlation between phenolics, proanthocyanidins and protein-precipitating constituents in mature foliage of six oak species. Oecologia 54:205–211

    Article  Google Scholar 

  • Matsuki M, MacLean SF (1994) Effects of different leaf traits on growth rates of insect herbivores on willows. Oecologia 100:141–152

    Article  Google Scholar 

  • McArt SH, Spalinger DE, Collins WB et al (2009) Summer dietary nitrogen availability as a potential bottom–up constraint on moose in South-central Alaska. Ecology 90:1400–1411

    Article  PubMed  Google Scholar 

  • McInnes PF, Naiman RJ, Pastor J, Cohen Y (1992) Effects of moose browsing on vegetation and litter of the boreal forest, Isle Royale. Ecology 73:2059–2075

    Article  Google Scholar 

  • McNaughton SJ (1976) Serengeti migratory wildebeest: facilitation of energy flow by grazing. Science 191:92–94

    Article  CAS  PubMed  Google Scholar 

  • McNaughton SJ (1983) Compensatory plant growth as a response to herbivory. Oikos 40:329–336

    Article  Google Scholar 

  • McNaughton SJ (1984) Grazing lawns: animals in herds, plant form, and coevolution. Am Nat 124:863–886

    Article  Google Scholar 

  • Miler O, Straile D (2010) How to cope with a superior enemy? Plant defence strategies in response to annual herbivore outbreaks. J Ecol 98:900–907. doi:10.1111/j.1365-2745.2010.01674.x

    Article  Google Scholar 

  • Molvar EM, Bowyer RT, Van Ballenberghe V, Van Brauenberone V (1993) Moose herbivory, browse quality, and nutrient cycling in an Alaskan treeline community. Oecologia 94:472–479

    Article  Google Scholar 

  • Mortimer GB, Ahlgren HL (1936) Influence of fertilization, irrigation, and stage and height of cutting on yield and composition of Kentucky blue-grass. J Am Soc Agron 28:515–533

    Article  CAS  Google Scholar 

  • Person BT, Herzog MP, Ruess RW, Sedinger JS (2003) Feedback dynamics of grazing lawns: coupling vegetation change with animal growth. Oecologia 135:583–592. doi:10.1007/s00442-003-1

    Article  PubMed  Google Scholar 

  • Peterson SL, Rockwell RF, Witte CR, Koons DN (2013) The legacy of destructive snow goose foraging on supratidal marsh habitat in the Hudson Bay lowlands. Arct Antarct Alp Res 45:575–583

    Article  Google Scholar 

  • Price PW (1991) The plant vigor hypothesis and herbivore attack. Oikos 62:244–251

    Article  Google Scholar 

  • Radtke A, Mosner E, Leyer I (2011) Vegetative reproduction capacities of floodplain willows—cutting response to competition and biomass loss. Plant Biol 14:257–264. doi:10.1111/j.1438-8677.2011.00509.x

    Article  PubMed  Google Scholar 

  • Roininen H, Price PW, Tahvanainen J (1988) Field test of resource regulation by the bud-galling sawfly, Euura mucronata, on Salix cinerea. Holarct Ecol 11:136–139. doi:10.1111/j.1600-0587.1988.tb00791.x

    Google Scholar 

  • Rosenthal JP, Kotanen PM (1994) Terrestrial plant tolerance to herbivory. Trends Ecol Evol 9:145–148. doi:10.1016/0169-5347(94)90180-5

    Article  CAS  PubMed  Google Scholar 

  • Ruess RW, Hendrick RL, Bryant JP (1998) Regulation of fine root dynamics by mammalian browsers in early successional Alaskan Taiga Forests. Ecology 79:2706–2720

    Article  Google Scholar 

  • Scott SL, Aarssen LW (2013) Leaf size versus leaf number tradeoffs in dioecious angiosperms. J Plant Ecol 6:29–35. doi:10.1093/jpe/rts029

    Article  Google Scholar 

  • Silber M, Davitt B (2000) Preparative binding of coomassie brilliant blue to bovine serum albumine at alkaline pH. Prep Biochem Biotechnol 30:209–229

    Article  CAS  PubMed  Google Scholar 

  • Singer FJ, Zeigenfuss LC, Cates RG et al (1998) Elk, multiple factors, and persistence of willows in National Parks. Wildl Soc Bull 26:419–428

    Google Scholar 

  • Stewart KM, Bowyer RT, Ruess RW et al (2006) Herbivore optimization by North American Elk: consequences for theory and management. Wildl Monogr 167:1–24

    Article  Google Scholar 

  • Tape KD, Lord R, Marshall H-P, Ruess RW (2010) Snow-mediated ptarmigan browsing and shrub expansion in arctic Alaska. Ecoscience 17:186–193. doi:10.2980/17-2-3323

    Article  Google Scholar 

  • Vaughton G, Ramsey M (1998) Sources and consequences of seed mass variation in Banksia marginata (Proteaceae). J Ecol 86:563–573

    Article  Google Scholar 

  • Wandera AJL, Richards JH, Mueller RJ (1992) The relationships between relative growth rate, meristematic potential and compensatory growth of semiarid-land shrubs. Oecologia 90:391–398

    Article  Google Scholar 

  • Wang J, Fang Y, Klaus S, Sun Y-H (2011) Winter foraging strategy of the Chinese Grouse (Bonasa sewerzowi): ecological and physiological factors. J Ornithol 153:257–264. doi:10.1007/s10336-011-0717-y

    Article  Google Scholar 

  • Weeden RB (1964) Spatial separation of sexes in rock and willow ptarmigan in winter. Auk 81:534–541

    Article  Google Scholar 

  • Welch B (1947) The generalization of student’s problem when several different population variances are involved. Biometrika 34:28–35

    CAS  PubMed  Google Scholar 

  • West G, Meng M (1966) Nutrition of willow ptarmigan in Northern Alaska. Auk 83:603–615

    Article  Google Scholar 

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Acknowledgments

We thank Stephen Sparrow and Darlene Massiak at the University of Alaska Fairbanks (UAF) School of Natural Resources for maintaining willow exclosures and facilitating the browsing simulation experiment. We thank the Calvin J. Lensink Foundation, the Arctic Institute of North America, and the UAF Graduate School for funding. Lola Oliver, Bruce Davitt, and Betty Blatner analyzed samples, and Knut Kielland and Perry Barboza provided valuable advice and help with sample preparation. Sophie Gilbert helped with the willow measurements. We would also like to thank Mark Lindberg, Joel Schmutz, Christa Mulder, and anonymous reviewers for valuable comments on the manuscript.

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Correspondence to Katie S. Christie.

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Communicated by Colin Mark Orians.

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Christie, K.S., Ruess, R.W. Experimental evidence that ptarmigan regulate willow bud production to their own advantage. Oecologia 178, 773–781 (2015). https://doi.org/10.1007/s00442-015-3265-y

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