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Scale dependence shapes how plant traits differentially affect levels of pre- and post-dispersal seed predation in Scots pine

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Abstract

To understand the demographic consequences of seed predation, it is essential to scale-up losses over space and time. We tested how individual tree characteristics, forest attributes, and the local environment affected rates of both pre- and post-dispersal seed predation in Scots pine Pinus sylvestris, in Scotland’s ancient native pinewoods. The sampling strategy was hierarchical, allowing assessment of how the influence of these factors differed with spatial scale. This approach revealed that the fate of a tree’s seeds depended on many factors, at multiple scales. Levels of seed predation were highly variable over space and time. Seed predation by local post-dispersal seed predators (invertebrates and small mammals) varied at the finest spatial scales, whereas mobile avian pre-dispersal seed predators discriminated among seeds at every spatial scale. Tree crown shape affected removal of seed by all seed predators; both crossbills Loxia spp. and generalist avian granivores selected trees with broad crowns. However, trees with narrow crowns were selected by red squirrels Sciurus vulgaris, and the associated tall understory vegetation supported the highest levels of post-dispersal seed predation. Seed chemistry was an effective seed defence that reduced seed loss to all seed predators. In contrast, increases in physical cone defence were ineffective at reducing seed loss and showed a potential trade-off with investment in seed viability. Large seeds carried a survival cost, being preferentially consumed by squirrels and post-dispersal seed predators. All post-dispersal seed predators consumed a higher proportion of seeds at the times and locations where seed fall was greatest.

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References

  • Alvarez-Espino R, Rios-Casanova L, Godinez-Alvarez H (2016) Seed removal in a tropical North American desert: an evaluation of pre- and post-dispersal seed removal in Stenocereus stellatus. Plant Biol 19:469–474

    Article  CAS  Google Scholar 

  • Benkman CW (1987) Food profitability and the foraging ecology of crossbills. Ecol Monogr 57:251–267

    Article  Google Scholar 

  • Benkman CW, Siepielski AM (2004) A keystone selective agent? Pine squirrels and the frequency of serotiny in lodgepole pine. Ecology 85:2082–2087

    Article  Google Scholar 

  • Benkman CW, Parchman TL, Favis A, Siepielski AM (2003) Reciprocal selection causes a coevolutionary arms race between crossbills and lodgepole pine. Am Nat 162:182–194

    Article  PubMed  Google Scholar 

  • Bennett KD (1984) The post-glacial history of Pinus sylvestris in the British Isles. Quat Sci Rev 3:133–155

    Article  Google Scholar 

  • Blendinger PG, Diaz-Velez MC (2010) Experimental field test of spatial variation in rodent predation of nuts relative to distance and seed density. Oecologia 163:415–423

    Article  PubMed  Google Scholar 

  • Blythe RM, Smyser TJ, Swihart RK (2015) Tree squirrel seed predation patterns may influence American chestnut restoration success. New For 46:593–600

    Article  Google Scholar 

  • Bock CE, Lepthien LW (1976) Synchronous eruptions of boreal seed-eating birds. Am Nat 110:559–571

    Article  Google Scholar 

  • Borthwick AW (1906) The life-history of Pinus sylvestris. Trans R Engl Arboric Soc 6:205–223

    Google Scholar 

  • Brown J (1992) GLIMMIX macro. In: Cary NC (ed) 8.0 SAS Institute Inc., USA

  • Calama R, Montero G (2007) Cone and seed production from stone pine (Pinus pinea L.) stands in Central Range (Spain). Eur J For Res 126:23–35

    Article  Google Scholar 

  • Carlisle A, Brown AHF (1968) Biological Flora of the British Isles: Pinus sylvestris L. J Ecol 56:269–307

    Article  Google Scholar 

  • Castro J, Gómez JM, García D, Zamora R, Hódar JA (1999) Seed predation and dispersal in relict Scots pine forests in southern Spain. Plant Ecol 145:115–123

    Article  Google Scholar 

  • Cattell RB (1966) The scree test for the number of factors. Multivar Behav Res 1:245–276

    Article  CAS  Google Scholar 

  • Cornelius JM, Hahn TP (2012) Seasonal pre-migratory fattening and increased activity in a nomadic and irruptive migrant, the Red Crossbill Loxia curvirostra. Ibis 154:693–702

    Article  Google Scholar 

  • Crist TO, Wiens JA (1994) Scale effects of vegetation on forager movement and seed harvesting by ants. Oikos 69:37–46

    Article  Google Scholar 

  • Debain S, Curt T, Lepart J, Prevosto B (2003) Reproductive variability in Pinus sylvestris in southern France: implications for invasion. J Veg Sci 14:509–516

    Article  Google Scholar 

  • Debeaujon I, Lepiniec L, Pourcel L, Routaboul J-M (2007) Seed coat development and dormancy. In: Bradford KJ, Nonogaki H (eds) Seed development, dormancy and germination. Blackwell, Oxford, pp 25–49

    Chapter  Google Scholar 

  • Eccard JA, Pusenius J, Sundell J, Halle S, Ylonen H (2008) Foraging patterns of voles at heterogeneous avian and uniform mustelid predation risk. Oecologia 157:725–734

    Article  Google Scholar 

  • Figueroa JA, Munoz AA, Mella JE, Arroyo MTK (2002) Pre- and post-dispersal seed predation in a mediterranean-type climate montane sclerophyllous forest in central Chile. Aust J Bot 50:183–195

    Article  Google Scholar 

  • Forestry Authority (1994) Caledonian pinewood inventory. Public Information Division, Forestry Commission, Edinburgh

    Google Scholar 

  • Forsyth DM, Wilson DJ, Easdale TA, Kunstler G, Canham CD, Ruscoe WA, Wright EF, Murphy L, Gormley AM, Gaxiola A, Coomes DA (2015) Century-scale effects of invasive deer and rodents on the dynamics of forests growing on soils of contrasting fertility. Ecol Monogr 85:157–180

    Article  Google Scholar 

  • Garcia D, Zamora R, Amico GC (2011) The spatial scale of plant–animal interactions: effects of resource availability and habitat structure. Ecol Monogr 81:103–121

    Article  Google Scholar 

  • Garcia-del-Rey E, Nanos N, Lopez-de-Heredia U, Gil Munoz P, Otto R, Maria Fernandez-Palacios J, Gil L (2011) Spatiotemporal variation of a Pinus seed rain available for an endemic finch in an insular environment. Eur J Wildl Res 57:337–347

    Article  Google Scholar 

  • Gibb JA (1958) Predation by tits and squirrels on the Eucosmid Ernarmonia conicolana (Heyl). J Anim Ecol 27:375–396

    Article  Google Scholar 

  • Gong H, Tang C, Wang B (2015) Post-dispersal seed predation and its relations with seed traits: a thirty-species-comparative study. Plant Species Biol 30:193–201

    Article  Google Scholar 

  • Hancock MH, Summers RW, Amphlett A, Willi J (2009) Testing prescribed fire as a tool to promote Scots pine Pinus sylvestris regeneration. Eur J For Res 128:319–333

    Article  Google Scholar 

  • Herrera CM, Jordano P, Guitian J, Traveset A (1998) Annual variability in seed production by woody plants and the masting concept: reassessment of principles and relationship to pollination and seed dispersal. Am Nat 152:576–594

    Article  CAS  PubMed  Google Scholar 

  • Hulme PE (1993) Post-dispersal seed predation by small mammals. Symp Zool Soc Lond 65:269–287

    Google Scholar 

  • Hulme PE (1996) Natural regeneration of yew (Taxus baccata L.): microsite, seed or herbivore limitation? J Ecol 84:853–861

    Article  Google Scholar 

  • Hulme PE (1998) Post-dispersal seed predation: consequences for plant demography and evolution. Perspect Plant Ecol Evol Syst 1:32–46

    Article  Google Scholar 

  • Hulme PE, Benkman CW (2001) Granivory. In: Herrera CM, Pellmyr O (eds) Plant–animal interactions. Blackwell, Oxford, pp 132–154

    Google Scholar 

  • Hulme PE, Kollmann J (2005) Seed predator guilds, spatial variation in post-dispersal seed predation and potential effects on plant demography—a temperate perspective. In: Forget PM, Lambert JE, Hulme PE, Vander Wal SB (eds) Seed fate. Predation, dispersal and seedling establishment. CABI Publishing, Wallingford, pp 9–30

    Chapter  Google Scholar 

  • Iason GR, O’Reilly-Wapstra JM, Brewer MJ, Summers RW, Moore BD (2011) Do multiple herbivores maintain chemical diversity of Scots pine monoterpenes? Phil Trans R Soc B 366:1337–1345

    Article  PubMed  Google Scholar 

  • IUCN (2018) The IUCN Red List of Threatened Species. Version 2018. http://www.iucnredlist.org. Downloaded on 09 Oct 2018

  • Janzen DH (1969) Seed-eaters versus seed size, number, toxicity and dispersal. Evolution 23:1–27

    Article  Google Scholar 

  • Janzen DH (1971) Seed predation by animals. Annu Rev Ecol Sys 2:465–493

    Article  Google Scholar 

  • Jardine DC (1992) Crossbills in Scotland 1990—an invasion year. Scottish Bird Report 23:65–69

    Google Scholar 

  • Jones IM, Koptur S, Gallegos HR, Tardanico JP, Trainer PA, Pena J (2017) Changing light conditions in pine rockland habitats affect the intensity and outcome of ant–plant interactions. Biotropica 49:83–91

    Article  Google Scholar 

  • Keeley JE (2012) Ecology and evolution of pine life histories. Ann For Sci 69:445–453

    Article  Google Scholar 

  • Lamont BB, Lemaitre DC, Cowling RM, Enright NJ (1991) Canopy seed storage in woody-plants. Bot Rev 57:277–317

    Article  Google Scholar 

  • Lobo N (2014) Conifer seed predation by terrestrial small mammals: a review of the patterns, implications, and limitations of top-down and bottom-up interactions. For Ecol Mgmt 328:45–54

    Article  Google Scholar 

  • Losada JM, Blanco-Moure N, Leslie AB (2018) Not all ‘pine cones’ flex: functional trade-offs and the evolution of seed release mechanisms. New Phytol. https://doi.org/10.1111/nph.15563

    Article  PubMed  Google Scholar 

  • Mallinson JR (1999) The impact of herbivores on the natural regeneration of temperate deciduous woodland. Department of Biological Sciences, University of Durham, Durham, p 202

    Google Scholar 

  • Maron JL, Crone E (2006) Herbivory: effects on plant abundance, distribution and population growth. Proc R Soc Lond B Biol Sci 273:2575–2584

    Article  Google Scholar 

  • Marquiss M (2002) Common crossbill Loxia curvirostra / Scottish crossbill Loxia scotica / Parrot crossbill Loxia pytopsittacus. In: Wernham C, Toms M, Marchant J, Clark J, Siriwadena G, Bailey S (eds) The migration atlas: movements of the birds of Britain and Ireland. T&A.D. Poyser, London, pp 663–665

    Google Scholar 

  • McVean DN (1963) Ecology of Scots pine in the Scottish highlands. J Ecol 51:657–670

    Article  Google Scholar 

  • Milesi FA, De Casenave JL, Cueto VR (2008) Selection of foraging sites by desert granivorous birds: vegetation structure, seed availability, species-specific foraging tactics, and spatial scale. Auk 125:473–484

    Article  Google Scholar 

  • Mittelbach GG, Gross KL (1984) Experimental studies of seed predation in old fields. Oecologia 65:7–13

    Article  PubMed  Google Scholar 

  • Mohamedyasseen Y, Barringer SA, Splittstoesser WE, Costanza S (1994) The role of seed coats in seed viability. Bot Rev 60:426–439

    Article  Google Scholar 

  • Molinari A, Wauters LA, Airoldi G, Cerinotti F, Martinoli A, Tosi G (2006) Cone selection by Eurasian red squirrels in mixed conifer forests in the Italian Alps. Acta Oecol 30:1–10

    Article  Google Scholar 

  • Moller H (1983) Foraging strategies of red squirrels (Sciurus vulgaris L.) in a Scots pine (Pinus sylvestris) plantation. University of Aberdeen, Aberdeen

  • Moller H (1986) Red squirrels (Sciurus vulgaris) feeding in a Scots pine plantation in Scotland. J Zool 209:61–83

    Article  Google Scholar 

  • Morris SA, Thompson HM (2011) Dehusking of seed by small mammals: default values for use in risk assessment. Integr Environ Assess Manag 7:147–148

    Article  PubMed  Google Scholar 

  • Muscolo A, Panuccio MR, Sidari M (2001) The effect of phenols on respiratory enzymes in seed germination. Plant Growth Regul 35:31–35

    Article  CAS  Google Scholar 

  • Myczko L, Benkman CW (2011) Great spotted woodpeckers Dendrocopos major exert multiple forms of phenotypic selection on Scots pine Pinus sylvestris. J Avian Biol 42:429–433

    Article  Google Scholar 

  • Myster RW (2003) Seed regeneration mechanisms over fine spatial scales on recovering Coffee plantation and pasture in Puerto Rico. Plant Ecol 166:199–205

    Article  Google Scholar 

  • Nadeau CP, Urban MC, Bridle JR (2017) Coarse climate change projections for species living in a fine-scaled world. Glob Chang Biol 23:12–24

    Article  PubMed  Google Scholar 

  • Nixon CJ, Cameron E (1994) A pilot study on the age structure and viability of the Mar Lodge Pinewoods. Scot For 48:22–27

    Google Scholar 

  • Nixon C, Clifford T (1994) The age and structure of native pinewood remnants. In: Aldhous JR (ed) Our pinewood heritage. Forestry Commission, RSPB, Scottish Natural Heritage, Culloden Academy, Inverness, pp 177–185

    Google Scholar 

  • Nystrand O, Granstrom A (1997) Post-dispersal predation on Pinus sylvestris seeds by Fringilla species: ground substrate affects selection for seed colour. Oecologia 110:353–359

    Article  CAS  PubMed  Google Scholar 

  • Nystrand O, Granstrom A (2000) Predation on Pinus sylvestris seeds and juvenile seedlings in relation to stand disturbance by logging. J Appl Ecol 37:449–463

    Article  Google Scholar 

  • Pennisi E (2007) Variable evolution. Science 316:686–687

    Article  CAS  PubMed  Google Scholar 

  • Perea R, Venturas M, Gil L (2014) Seed predation on the ground or in the tree? Size-related differences in behavior and ecology of granivorous birds. Acta Ornithol 49:119–130

    Article  Google Scholar 

  • Peterken GF (1996) Natural woodland. Cambridge University Press, Cambridge, p 17

    Google Scholar 

  • Petty SJ, Lurz PWW, Rushton SP (2003) Predation of red squirrels by northern goshawks in a conifer forest in northern England: can this limit squirrel numbers and create a conservation dilemma? Biol Conserv 111:105–114

    Article  Google Scholar 

  • Price ML, Butler LG (1977) Rapid visual estimation and spectrophotometric determination of tannin content of Sorghum grain. J Agric Food Chem 25:1268–1273

    Article  CAS  Google Scholar 

  • Pullianen E, Lajunen L (1984) Chemical composition of Pices abies and Pinus sylvestris seeds under subarctic conditions. Can J For Res 14:214–217

    Article  Google Scholar 

  • Ramos-Palacios CR, Badano EI, Flores J, Flores-Cano JA, Flores-Flores JL (2014) Distribution patterns of acorns after primary dispersion in a fragmented oak forest and their consequences on predators and dispersers. Eur J For Res 133:391–404

    Article  Google Scholar 

  • Roques A, Skrzypczyńska M (2003) Seed-infesting chalcids of the genus Megastigmus Dalman, 1820 (Hymenoptera: Torymidae) native and introduced to the West Palearctic region: taxonomy, host specificity and distribution. J Nat Hist 37:127–238

    Article  Google Scholar 

  • RSPB (1993) Time for pine: a future for Caledonian pinewoods. RSPB, Sandy

    Google Scholar 

  • Ruano I, del Peso C, Bravo F (2015) Post-dispersal predation of Pinus pinaster Aiton seeds: key factors and effects on belowground seed bank. Eur J For Res 134:309–318

    Article  Google Scholar 

  • Saatkamp A, Cochrane A, Commander L, Guja Lydia K, Jimenez-Alfaro B, Larson J, Nicotra A, Poschlod P, Silveira FAO, Cross Adam T, Dalziell EL, Dickie J, Erickson TE, Fidelis A, Fuchs A, Golos PJ, Hope M, Lewandrowski W, Merritt DJ, Miller BP, Miller Russell G, Offord CA, Ooi MKJ, Satyanti A, Sommerville KD, Tangney R, Tomlinson S, Turner S, Walck JL (2018) A research agenda for seed-trait functional ecology. New Phytol 221:1764–1775

    Article  PubMed  Google Scholar 

  • Saracino A, D’Alessandro CM, Borghetti M (2004) Seed colour and post-fire bird predation in a Mediterranean pine forest. Acta Oecol 26:191–196

    Article  Google Scholar 

  • SAS II (2000) SAS OnlineDoc®, version 8

  • Saska P, Martinkova Z, Honek A (2010) Temperature and rate of seed consumption by ground beetles (Carabidae). Biol Control 52:91–95

    Article  Google Scholar 

  • Sheffield LM, Crait JR, Edge WD, Wang GM (2001) Response of American kestrels and gray-tailed voles to vegetation height and supplemental perches. Can J Zool 79:380–385

    Article  Google Scholar 

  • Shimada T, Saitoh T (2006) Re-evaluation of the relationship between rodent populations and acorn masting: a review from the aspect of nutrients and defensive chemicals in acorns. Popul Ecol 48:341–352

    Article  Google Scholar 

  • Skinner GJ, Allen GW (1996) Ants. The Richmond Publishing Co. Limited, Slough

    Google Scholar 

  • Skłodowski J, Bajor P, Trynkos M (2018) Carabids benefit more from pine stands with added understory or second story of broad-leaved trees favored by climate change than from one-storied pine stands. Eur J For Res 137:745–757

    Article  CAS  Google Scholar 

  • Smith CC (1970) Coevolution of pine squirrels (Tamiasciurus) and conifers. Ecol Monogr 40:349–371

    Article  Google Scholar 

  • Steen R, Barmoen M (2017) Diel activity of foraging Eurasian red squirrels (Sciurus vulgaris) in the winter revealed by camera traps. Hystrix It J Mamm 28:43–47

    Google Scholar 

  • Steven HM, Carlisle A (1959) The native pinewoods of Scotland. Oliver and Boyd, Edinburgh

    Google Scholar 

  • Stokstad E (2016) Red squirrels rising. Science 352:1268–1271

    Article  CAS  PubMed  Google Scholar 

  • Summers RW (2007) Stand selection by birds in Scots pinewoods in Scotland: the need for more old-growth pinewood. Ibis 149:175–182

    Article  Google Scholar 

  • Summers RW (2011) Patterns of exploitation of annually varying Pinus sylvestris cone crops by seed-eaters of differing dispersal ability. Ecography 34:723–728

    Article  Google Scholar 

  • Summers RW (2018) Abernethy forest: the history and ecology of an old Scottish pinewood. Centre for Conservation Science, Royal Society for the Protection of Birds, Inverness

    Google Scholar 

  • Summers R, Piertney SB (2003) The Scottish Crossbill—what we know and what we don’t. Br Birds 96:100–111

    Google Scholar 

  • Summers RW, Proctor R (1999) Tree and cone selection by crossbills Loxia sp. and red squirrels Sciurus vulgaris at Abernethy forest, Strathspey. For Ecol Manag 118:173–182

    Article  Google Scholar 

  • Summers RW, Proctor R (2005) Timing of shedding seeds and cones, and production in different stands of Scots pines at Abernethy Forest, Scotland. Forestry 78:541–549

    Article  Google Scholar 

  • van der Meij MAA, Bout RG (2006) Seed husking time and maximal bite force in finches. J Exp Biol 209:3329–3335

    Article  PubMed  Google Scholar 

  • Wang Z, Zhang Y, Zhang D, Li J, Yi X (2016) Nutritional and defensive properties of Fagaceae nuts dispersed by animals: a multiple species study. Eur J For Res 135:911–917

    Article  CAS  Google Scholar 

  • Wang B, Phillips JS, Tomlinson KW (2018) Tradeoff between physical and chemical defense in plant seeds is mediated by seed mass. Oikos 127:440–447

    Article  CAS  Google Scholar 

  • Wauters L, Dhondt AA (1992) Spacing behaviour of red squirrels, Sciurus vulgaris: variation between habitats and the sexes. Anim Behav 43:297–311

    Article  Google Scholar 

  • Weidner S, Amarowicz R, Karamać M, Frączek E (2000) Changes in endogenous phenolic acids during development of Secale cereale caryopses and after dehydration treatment of unripe rye grains. Plant Physiol Biochem 38:595–602

    Article  CAS  Google Scholar 

  • Worthy FR, Law R, Hulme PE (2006) Modelling the quantitative effects of pre- and post-dispersal seed predation in Pinus sylvestris L. J Ecol 94:1201–1213

    Article  Google Scholar 

  • Xiao Z, Mi X, Holyoak M, Xie W, Cao K, Yang X, Huang X, Krebs CJ (2017) Seed-predator satiation and Janzen–Connell effects vary with spatial scales for seed-feeding insects. Ann Bot 119:109–116

    Article  PubMed  Google Scholar 

  • Xistras D (1980) Seed production and quality and early growth of seedlings in the native pinewoods at Glentanar. Department of Forestry, University of Aberdeen, Aberdeen, p 192

    Google Scholar 

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Acknowledgements

Mick Marquiss and Richard Law made valuable contributions throughout this study. The Royal Society for the Protection of Birds permitted fieldwork at Abernethy, provided accommodation, and many staff gave useful advice. Scottish Natural Heritage permitted fieldwork at Mar Lodge and provided accommodation. Ron Summers and Robert Proctor provided additional data on cone counts for Abernethy Forest. Statistical advice was provided by David Elston. This research was funded by a Natural Environment Research Council studentship to FRW (Grant No. NER/S/A/2002/11035) and while writing by a Yunnan Provincial Post-doctoral Grant to FRW.

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Map of study sites (PDF 450 kb)

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Forest structure (PDF 178 kb)

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Timeline of seed development and seed predation (PDF 119 kb)

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Sectors marked for cone collection (XLSX 20 kb)

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Supplementary methods (PDF 122 kb)

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Common factor analysis (PDF 204 kb)

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Supplementary results (PDF 210 kb)

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Worthy, F.R., Hulme, P.E. Scale dependence shapes how plant traits differentially affect levels of pre- and post-dispersal seed predation in Scots pine. Eur J Forest Res 138, 653–672 (2019). https://doi.org/10.1007/s10342-019-01198-y

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