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88Y. Du et al. / Acta Oecologica 39 (2012) 87e93are caused by the increased litter inputs after the storm, whichmay kill seedlings already present, inhibit germination bycovering seeds, and prevent seedling establishment (Uriarte et al.,2005). Ice storm damage to tree crowns could also decrease and/or delay seed production in the short term, as self-preservationagainst extreme storm conditions consumes stored reserves. Inthis case, seed rain will contribute little to new recruitment, andseed and seedling banks would be the major sources of regeneration.Ice storm events could also lead to changes in patterns offruit production, which would likely affect dispersers’ abundanceand behavior due to the loss of food resources. Moreover,increased light penetration through the damaged canopy to thesoil surface may kill seeds before germination or desiccateexisting seedlings.Conversely, positive effects may be due to increased lightpenetration, which would stimulate seed germination from theseed bank and the growth of seedlings present in the seedling bank,while increased litter inputs could also enhance nutrient supply(Lomascolo and Aide, 2001; Uriarte et al., 2005). In addition, icestorms may be expected to lead to weaker negative densitydependenteffects of seedling survival, as extra light could permitseedlings to resist pathogens and herbivores and thereby increasesurvival, which has significant implications for both seedlingsurvival and species coexistence. Understanding how ice stormsinfluence seed production and seedling recruitment is essential tothe prediction of the long-term effects of natural disturbance onsubtropical forest dynamics and species richness.Many previous studies of ice storms in forests have concentratedon the susceptibility of tree species to ice damage (Siccama et al.,1976; Seischab et al., 1993). Others have focused on the influenceof elevation (Downs, 1938; Nicholas and Zedaker, 1989), slope(Rhoades, 1995; Rebertus et al., 1997), and topography (Rebertuset al., 1997; Mou and Warrillow, 2000) on ice deposition, and onthe response of forest understory seedling/sapling density to majorice storms (Darwin et al., 2004). To our knowledge, no previousstudies have investigated the effects of ice storms on seedproduction.Because seedling data is largely unavailable, we focused here onthe seed rain phase. The major objective of our study was to explorethe effect of ice storm damage on seedfall, and investigate whetherthe degree of seed limitation is correlated with dispersal modes.We evaluated the following hypotheses:1) Seed production after the storm is less than that before thestorm, as self-preservation against extreme storm conditionsconsumes stored reserves;2) Seed limitation after the storm is more severe than before thestorm, as a consequence of decreased seed production;2. Material and methods2.1. Study siteThe study was conducted in a 24-ha permanent forest plot(29 15.101 0 -29 15.344 0 N, 118 07.010 0 e118 07.400 0 E) in GutianshanNational Nature Reserve (GNNR), Kaihua County, Zhejiang Provincein eastern China. GNNR covers a total area of approximately8107 ha. Mountains with steep slopes characterize the topography.The substrate consists mainly of granite. The mean annualtemperature is 15.3 C. The hottest month is July with a meantemperature of 27.9 C, and the coldest is January with a meantemperature of 4.3 C. The mean annual precipitation is 1787 mmwith seasonal distribution over the year (Yu et al., 2001). A total of1991 vascular plant species, belonging to 244 families and 897genera, have been recorded within the entire GNNR (Chen andFeng, 2002; Hu et al., 2003).2.2. Methods2.2.1. Description of plotIn 2005, the Gutianshan permanent plot (GTS) covering 24-ha(400 600 m, horizontal distance) was established within theevergreen broad-leaved forest in GNNR. Data were collectedfollowing the standard census protocol of the CTFS (Center forTropical Forest Science) network (Condit, 1998). The elevationrange between the highest and lowest points in the plot was 269 m(from 446 m to 715 m). The soil was a subtropical red soil (equivalentto Ultisols in US soil taxonomy) (Zhang et al., 2011). The firsttree census was conducted in 2005. All woody stems 1 cm in DBHwere mapped, measured, identified, and tagged (Legendre et al.,2009). There were a total of 140,700 individuals belonging to 159species in the plot. The dominant species were Castanopsis eyrei(Fagaceae), Schima superba (Theaceae) and Pinus massoniana(Pinaceae) (Zhang et al., 2011).2.2.2. Seed collectionSeed rain has been censused weekly since June 2006, using 130seed traps set along 2.3 km of trails within the plot (Du et al., 2009).As the ice storm destroyed all seed traps in February 2008, we reestablishedall seed traps in March and April of 2008 in theiroriginal sites. We resumed weekly collections in May 2008. Eachseed trap consisted of a square, 0.5 m 2 PVC frame supportinga shallow, open-topped, 1-mm nylon mesh bag suspended 0.8 mabove the ground on four PVC posts. All seeds, fruits, seed-bearingfruit fragments, flowers, capsules, and other reproductive parts ofplants that fell into the traps were identified to species and recorded.Fruits were categorized as aborted, immature, damaged,fragments and mature (Wright and Calderón, 1995; Wright et al.,1999). Because the seed traps were located above the ground,they captured fruits and falling seeds directly from trees, as well asthose spat or defecated by birds, bats and arboreal mammals; theydid not, however, record secondary dispersal by rodents and otherterrestrial animals (Muller-Landau et al., 2008). All data presentedrefer to seed number, based upon either a count of actual seeds perfruit, or calculated based upon the mean number of seeds per fruit.Dispersal mode was assigned to each species based on fruitmorphology (Du et al., 2009). Each plant species was assigned toone main dispersal mode. Fruit morphology was the basis forclassifying species as dispersed by wind, animals, or explosion(Table 1).2.2.3. Data analysis2.2.3.1. Calculation of recruitment limitation. We calculatedmeasures of seed limitation, source limitation and dispersal limitation(Clark et al., 1998; Nathan and Muller-Landau, 2000; Muller-Landau et al., 2002) for periods of 20 months before and after theice storm using data on seed arrival into the 130 seed traps in theplot. Seed limitation refers to the failure of seeds to arrive at allsuitable sites (Eriksson and Ehrlen, 1992; Turnbull et al., 2000).Fundamental seed limitation is defined as 1 ða=nÞ, where a is thenumber of seed traps reached by seeds and n is the total number ofseed traps. Thus, seed limitation can arise from limited seednumbers and limited dispersal of available seeds (Muller-Landauet al., 2002). Source limitation is the failure of seeds to reach sitesdue simply to insufficient seed numbers: there are not enoughseeds to go around, even if all seeds are uniformly distributedamong sites (Clark et al., 1998). Source limitation (stochastic) can bedefined as expð ðs=nÞÞ, where s is total seed number arriving alltraps. Non-uniform distribution of seeds is nearly ubiquitous,191
Y. Du et al. / Acta Oecologica 39 (2012) 87e93 89Table 1Demographic characteristics of 62 species whose seeds were collected during the 40-month period (T, tree; S, shrub). Dispersers are from Du et al. (2009), and Teng Fang(unpublished data). Pre-/post-seed density is the density of seeds 20 months before and 20 months after the ice storm. Pre-/post-seed limitation, pre-/post-source limitation,and pre-/post-dispersal limitation are the limitation 20 months before and 20 months after the ice storm. IV is the abbreviation of important value. Abundance is the totalindividual number in 24 ha plot. Table was sorted by the pre-seed density.SpeciesLifehistoryDispersersIVrankPre-seeddensity(m 2 )Post-seeddensity(m 2 )Pre-seedlimitationPost-seedlimitationPre-sourcelimitationPost-sourcelimitationPre-dispersallimitationSchima superba T Wind 2 930.59 49.97 0.00 0.02 0.00 0.00 0.00 0.02Castanopsis eyrei T Rodents 1 55.34 4.42 0.27 0.65 0.00 0.11 0.27 0.61Fraxinus insularis T Wind 33 43.06 1.22 0.18 0.83 0.00 0.54 0.18 0.63Ilex micrococca T Birds 92 26.12 6.83 0.98 0.98 0.00 0.03 0.98 0.98Eurya muricata S Mammals, birds 4 24.86 243.94 0.88 0.74 0.00 0.00 0.88 0.74Quercus serrata T Rodents 25 16.02 12.31 0.73 0.71 0.00 0.00 0.73 0.71Toxicodendron succedaneum T or S Animals 38 15.91 12.86 0.07 0.42 0.00 0.00 0.07 0.42Pinus massoniana T Wind 23 10.97 26.29 0.07 0.01 0.00 0.00 0.07 0.01Rhododendron ovatum S Wind 3 10.54 15.78 0.97 0.98 0.01 0.00 0.97 0.98Ternstroemia gymnanthera T or S Birds 9 8.89 12.35 0.52 0.34 0.01 0.00 0.52 0.34Daphniphyllum oldhamii T or S Mammals, birds 8 7.82 2.49 0.45 0.67 0.02 0.29 0.44 0.54Vaccinium bracteatum T or S Mammals, birds 19 6.91 0.37 0.96 0.98 0.03 0.83 0.96 0.86Eurya rubiginosa S Birds 12 5.80 1.20 0.99 0.99 0.06 0.55 0.99 0.98Vaccinium carlesii S Mammals, birds 14 5.62 0.00 0.95 1.00 0.06 1.00 0.94 1.00Cyclobalanopsis gracilis T or S Rodents 125 5.46 0.15 0.93 0.98 0.07 0.93 0.93 0.69Alniphyllum fortunei T Wind 47 4.38 1.29 0.95 0.99 0.11 0.52 0.95 0.98Machilus thunbergii T Animals 22 3.02 0.18 0.89 0.96 0.22 0.91 0.86 0.56Cyclobalanopsis glauca T Animals 21 2.08 0.08 0.85 0.97 0.35 0.96 0.76 0.18Itea oblonga T or S wind 27 1.80 0.00 0.99 1.00 0.41 1.00 0.99 1.00Neolitsea aurata T Mammals 5 1.72 0.77 0.88 0.84 0.42 0.68 0.79 0.49Adinandra millettii T or S Animals 35 1.69 44.00 0.99 0.96 0.43 0.00 0.99 0.96Euonymus oblongifolius T or S Animals 114 1.69 0.00 0.98 1.00 0.43 1.00 0.96 1.00Corylopsis glandulifera S Explosive, Wind 34 1.58 0.55 0.94 0.93 0.45 0.76 0.89 0.71Rhododendron latoucheae S Wind 13 1.38 14.85 0.99 0.98 0.50 0.00 0.98 0.98Loropetalum chinense T or S Explosive, weight 10 1.08 1.58 0.83 0.83 0.58 0.45 0.59 0.69Lithocarpus glaber T Rodents 20 1.08 0.06 0.95 0.99 0.58 0.97 0.87 0.75Myrica rubra T Mammals, birds 24 0.74 2.97 0.95 0.94 0.69 0.23 0.83 0.92Idesia polycarpa T Animals 99 0.72 0.00 0.99 1.00 0.70 1.00 0.97 1.00Vaccinium mandarinorum T or S Mammals, birds 11 0.40 3.80 0.99 0.98 0.82 0.15 0.96 0.97Camellia chekiangoleosa T or S Mammals 7 0.22 0.05 0.98 0.99 0.90 0.98 0.77 0.66Albizia kalkora T Animals 44 0.17 0.14 0.93 0.99 0.92 0.93 0.15 0.88Dalbergia hupeana T Wind 48 0.15 0.05 0.98 0.99 0.93 0.98 0.69 0.66Distylium myricoides T or S Explosive 36 0.14 4.88 0.99 0.87 0.93 0.09 0.88 0.86Castanopsis fargesii T Rodents 29 0.11 0.00 0.99 1.00 0.95 1.00 0.85 1.00Camellia fraterna T or S Mammals 15 0.08 0.03 0.96 0.98 0.96 0.98 0.02 0.01Styrax dasyanthus S Animals 65 0.06 0.05 0.98 0.98 0.97 0.98 0.49 0.33Michelia skinneriana T Birds 70 0.06 0.00 0.99 1.00 0.97 1.00 0.75 1.00Malus leiocalyca T or S Rodents 56 0.05 0.02 0.99 0.99 0.98 0.99 0.66 0.00Euscaphis japonica T or S Birds 67 0.05 0.03 0.99 0.99 0.98 0.98 0.66 0.50Diospyros glaucifolia T Mammals 59 0.05 0.03 0.99 0.98 0.98 0.98 0.66 0.01Elaeocarpus decipiens T Animals 42 0.02 0.00 0.99 1.00 0.99 1.00 0.00 1.00Sloanea sinensis T Animals 101 0.02 0.02 0.99 0.99 0.99 0.99 0.00 0.00Nyssa sinensis T Animals 123 0.02 0.00 0.99 1.00 0.99 1.00 0.00 1.00Rhaphiolepis indica S Mammals, birds 17 0.02 0.46 0.99 0.94 0.99 0.79 0.00 0.70Rhododendron simsii S Animals 30 0.02 0.00 0.99 1.00 0.99 1.00 0.00 1.00Litsea coreana T Animals 32 0.00 0.06 1.00 0.99 1.00 0.97 1.00 0.75Wikstroemia monnula S Animals 81 0.00 0.18 1.00 0.99 1.00 0.91 1.00 0.91Symplocos anomala T or S Animals 61 0.00 0.17 1.00 0.99 1.00 0.92 1.00 0.91Syzygium buxifolium T or S Mammals, birds 16 0.00 5.23 1.00 0.82 1.00 0.07 1.00 0.80Photinia glabra T Animals 26 0.00 0.12 1.00 0.99 1.00 0.94 1.00 0.87Meliosma oldhamii T Animals 31 0.00 0.02 1.00 0.99 1.00 0.99 1.00 0.00Ilex elmerrilliana T Birds 39 0.00 0.12 1.00 0.99 1.00 0.94 1.00 0.87Osmanthus cooperi T or S Animals 60 0.00 0.14 1.00 0.98 1.00 0.93 1.00 0.65Platycarya strobilacea T or S Wind 73 0.00 0.69 1.00 0.99 1.00 0.71 1.00 0.97Magnolia cylindrica T Animals 108 0.00 0.06 1.00 0.99 1.00 0.97 1.00 0.75Rhododendron mariesii S Wind 50 0.00 5.54 1.00 0.99 1.00 0.06 1.00 0.99Manglietia yuyuanensis T Animals 102 0.00 0.12 1.00 0.98 1.00 0.94 1.00 0.74Symplocos sumuntia T Animals 87 0.00 0.26 1.00 0.98 1.00 0.88 1.00 0.87Lindera glauca T or S Animals 90 0.00 0.18 1.00 0.98 1.00 0.91 1.00 0.83Cleyera japonica T or S Birds 53 0.00 0.12 1.00 0.99 1.00 0.94 1.00 0.87Styrax odoratissimus T Animals 37 0.00 0.06 1.00 0.98 1.00 0.97 1.00 0.49Acer cordatum T or S Wind 41 0.00 0.48 1.00 0.88 1.00 0.79 1.00 0.42Post-dispersallimitationbecause seeds are dispersed limited distances from their sourcesand are often dispersed in clumps and because adult trees arethemselves clumped, increasing the number of sites that are veryfar from any sources (Ribbens et al., 1994). Clark et al. (1998)quantify dispersal limitation as1a=n1 source limitationTherefore, dispersal limitation depends not only on dispersalbut also on tree abundance and distribution, and on seed192
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