succession of bryophyte assemblages following clear-cut logging in boreal spruce-dominated forests...
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Succession of bryophyte assemblages followingclear-cut logging in boreal spruce-dominatedforests in south-central Sweden — Doesretrogressive succession occur?
Martin Schmalholz and Kristoffer Hylander
Abstract: The recovery process of boreal bryophyte communities after clear-cutting was studied in a chronosequence insouth-central Sweden. We hypothesized that high initial grass cover on clearcuts, high litter cover and low light levels dur-ing canopy closure, and shortage of coarse woody substrates would constrain recovery in different ways. Instead, both epi-geic and epixylic guilds (i.e., species growing on forest floor and deadwood) displayed a gradual increase in similarityover time from the clear-cut phase, perhaps because of the absence of distinct peaks in needle litter and canopy cover. Ep-ixylic species started to recover long before the accumulation of deadwood, indicating that microclimate rather than sub-strate availability was the most constraining factor during the first 50 years. Since we did not find any other bottlenecksduring the succession after clear-cutting, conservation measures aiming at decreasing local extinction rates during clear-cutting may also increase long-term persistence. On the other hand, as the results from the epixylic guild suggest, otherfactors during the forest succession, such as the development of a suitable microclimate, might be more important forsome organisms, thus possibly mitigating such long-term positive effects of adjusted management during the clear-cuttingoperation.
Resume : Le processus de recuperation des communautes boreales de bryophytes a la suite d’une coupe a blanc a ete etu-die le long d’une chronosequence dans le centre de la Suede. Nous avons fait l’hypothese que le couvert initial de hautesherbes dans les coupes a blanc, l’epaisse couche de litiere et le faible niveau de luminosite durant la fermeture du couvertainsi que la penurie de substrats ligneux grossiers devraient de diverses facons limiter la recuperation. Au contraire, tantles guildes epigees qu’epixyles (c.-a-d. les especes qui croissent respectivement sur la couverture morte et le bois mort)ont connu une augmentation similaire, graduelle avec le temps depuis la phase de la coupe a blanc, peut-etre a cause del’absence de pics distincts de production de litiere d’aiguilles et de fermeture du couvert. Les especes epixyles ont com-mence a recuperer bien avant l’accumulation de bois mort, indiquant que le microclimat plutot que la disponibilite du sub-strat etait le facteur le plus contraignant pendant les 50 premieres annees. Etant donne que nous n’avons observe aucunautre goulot d’etranglement pendant la succession apres la coupe a blanc, les mesures de conservation visant a reduire lestaux d’extinction locale pendant la coupe a blanc peuvent egalement accroıtre la persistance a long terme. D’autre part,comme l’indiquent les resultats de la guilde epixyle, d’autres facteurs tels que le developpement d’un microclimat appro-prie, pendant la succession forestiere, pourraient etre plus importants pour certains organismes et, par consequent, possible-ment attenuer de tels effets positifs a long terme de l’amenagement adapte durant les operations de coupe a blanc.
[Traduit par la Redaction]
IntroductionThe process of community assembly during succession in
terrestrial plant communities has traditionally been con-ceived as a linear and progressive recovery towards the pre-disturbance state (Whittaker 1953). However, under somecircumstances, for example, when stochastic influences dur-ing the recruitment phase are high (Frelich et al. 1993) orafter extreme disturbance episodes (Baker and Walford1995), some ecosystems will be prone to express multiple
successional trajectories. Several factors, such as dispersallimitation, environmental conditions, and competition, con-strain the assembly of species along the successional trajec-tory towards compositions typical of late seral communities(cf. Belyea and Lancaster 1999). It is possible that such fac-tors could not only act as filters, restricting the establish-ment of species during postdisturbance succession, but alsointroduce periods of retrogressive succession, that is, shiftstowards an earlier successional state, and hence create bot-tleneck episodes for certain organisms (cf. Wardle et al.2004).
To understand the long-term consequences of forestry onecosystem function and biodiversity, a comprehensiveunderstanding of the biotic response during the whole forestsuccession is needed. Today, stand-level biodiversity conser-vation in Fennoscandian forestry tends to focus on the initialeffects of clear-cutting through the use of adjusted harvest-ing methods such as structural retention of coarse woody de-
Received 24 November 2008. Accepted 2 July 2009. Publishedon the NRC Research Press Web site at cjfr.nrc.ca on 9 October2009.
M. Schmalholz1 and K. Hylander. Department of Botany,University of Stockholm, SE-106 91 Stockholm, Sweden.
1Corresponding author (e-mail:[email protected]).
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bris (CWD), snags, and live trees (Rosenvald and Lohmus2008). This prioritization seems fair considering the negativeeffects of clear-cutting on late successional forest commun-ities (e.g., Hannerz and Hanell 1997; Fenton et al. 2003).However, if the recovery of late successional forest com-munities displays retrogressive episodes during postharvestsuccession, conservation measures aiming solely at increas-ing the initial survival on the clearcuts may not be consid-ered a good long-term strategy. In this study, we explorethe successional trajectory of bryophytes in a chronose-quence after clear-cut logging with focus on possible rela-tionships to changes in both abiotic and biotic standconditions, which possibly might constrain the succession indifferent ways. Since mature managed boreal stands tend tohave rather similar species composition of bryophytes, webelieve that a careful stratification of sites according to pro-ductivity, moisture, and microtopography and the avoidanceof old stands makes the chronosequence approach appropri-ate in this case.
Understanding successional trajectories of bryophytes,that is, mosses and liverworts, is important considering theirhigh influence on the boreal forest ecosystem (e.g., DeLucaet al. 2002) as well as their unique contribution to under-story diversity (Esseen et al. 1997). Boreal bryophyte com-munities decrease dramatically in abundance after clear-cutting (e.g., Hylander et al. 2005) as a result of the highlyaltered microclimate (Keenan and Kimmins 1993). Data de-scribing the major pattern of bryophyte recovery followingclear-cut logging are however scarce.
In moderately productive Fennoscandian spruce forests,the grass species Deschampsia flexuosa L. usually domi-nates the field layer some years after clear-cutting becauseof its ability to resprout and rapidly expand (Bergstedt andMilberg 2001). Comparative studies performed in Finlandshow that this phase is more pronounced after clear-cuttingthan after fire (Uotila and Kouki 2005) because of the rela-tively shallow position of D. flexuosa rhizomes (Schimmeland Granstrom 1996). We hypothesize that the ongoing re-covery of forest floor bryophytes may be constrained bycompetition for space caused by a high cover of D. flexuosaand that species that survived the initial disturbance associ-ated with clear-cutting might be competitively excluded bythe grass. Several other characteristic stand features ofyoung managed forests might also be harmful to recoveringbryophyte communities. Prior to self-thinning or thinningoperations, that is, around 25–40 years after clear-cutting,maturing Picea abies stands can develop a dense standstructure with limited subcanopy light penetration(Johansson 1987). Although bryophytes generally are con-sidered to be shade tolerant and favored by canopy closure,bryophyte cover has been found to decrease in heavilyshaded stands (e.g., Rambo and Muir 1998). In addition,dense conifer stands usually develop a pronounced needlelayer on the forest floor because of conifer branches beingconstantly under the light compensation point (Johansson1987), in some places forming thick carpets on the forestfloor (K. Hylander, personal observation). Hence, we hy-pothesize that both forest floor and boulder-living bryo-phytes will display arrested recovery or even retrogressionduring this period because of high litterfall and low lightlevels.
Lastly, in addition to the very low amounts of CWD leftafter clear-cutting compared with natural disturbances, thecontinuous timber extraction during thinning may delay theaccumulation of new deadwood in managed forests. Sincewoody debris, especially large diameter classes of Norwayspruce (Kruys et al. 1999), is an important substrate formany bryophyte specialists, we suspect that the recoveryrate of the epixylic guild (e.g., species utilizing deadwood)will be constrained by substrate availability and hence showa substantial increase in recovery after 50 years, when newdeadwood is more likely to accumulate (Ekbom et al. 2006).
Here we investigate the bryophyte postlogging successionwith special emphasis on four potentially important factorsthat could constrain the postlogging recovery: (i) competi-tion from the expansive graminoid D. flexuosa on the clear-cuts, both (ii) high litter cover and (iii) low light levelsduring canopy closure, and (iv) shortage of CWD. We makeseparate analyzes for three bryophyte guilds: epigeics (i.e.,forest floor species), epilitics (i.e., boulder-living), and epi-xylic species.
Methods
Study areaThe present study was conducted in the Bergslagen re-
gion, which is a historically and culturally distinct region ofsouth-central Sweden (Fig. 1) famous for its mining industrythat flourished from the end of the 13th century until the be-ginning of the 20th century. Owing to the large demand forcharcoal for the melting of iron and copper ore, clear-cuttingbecame the most common logging method in this regionearlier (>200 years ago) than in other parts of Sweden(Nilsson 1996). Within the study area, management regimeshave been fairly constant over time, although the regular useof slash burning of clearcuts employed in the 1920s and1950s and the common practice of forest fertilizing in the1960s must be considered when the results are interpreted(Ostlund et al. 1997; Lars Ostlund, personal communication2009). The landscape is predominately forested with Nor-way spruce (Picea abies (L.) Karst.) on mesic-moist andmoderate-rich sites and Scots pine (Pinus sylvestris L.) ondrier, nutrient poor sites with a thin soil layer and on wet,peat-producing wetlands. The study area belongs to thesouthern boreal vegetation zone (sensu Ahti et al. 1968),and all stands are situated within the four counties of Varm-land, Orebro, Vastmanland, and Dalarna. The area has beensubjected to repeated glaciations during the Pleistoceneepoch, and sandy-loamy till derived from acidic granite bed-rock is the dominant soil type (Freden 1994). The highestpostglacial coastline is situated at *170–180 m above sealevel. The yearly precipitation in the area is between 800–1100 mm with increasing precipitation from east to west.The mean temperature is –7 8C for January and 14 8C forJuly (Raab and Vedin 1999).
Stand selection and sampling designWe selected 31 stands of different ages (2–96 years),
carefully stratified according to several environmental varia-bles (see below), to construct a chronosequence. The selec-tion of forest stands was carried out in a two-step procedure.In the initial step, we selected stands from two databases
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provided by the forest companies Sveaskog and BergvikSkog AB that conformed to the following five criteria: 1,slightly poor to moderate productivity (i.e., site index G22–G28 according to Hagglund and Lundmark 1999); 2, mesicmoisture conditions (i.e., dry and wet sites omitted); 3, treespecies composition dominated by Norway spruce (>50%basal area) with less than 15% deciduous trees; 4, regenera-tion after traditional clear-cutting; and 5, low to intermediatecover of boulders (0%–7.5%). In the second step, all siteswere visited prior to data collection to validate the initial se-lection step. When checked in the field, approximately onethird of all stands selected during the initial selection stepdid not conform to our criteria and were hence omitted. Ineach stand, a rectangular 50 m � 20 m plot, divided into ten10 m � 10 m subplots was established in a representativepart of the stand at least 25 m from the nearest stand edge.
Data collectionThe field data were collected over two periods in 2007
(16 July – 2 August and 10–28 September) and in 2008(10–24 July). Canopy cover was estimated visually as oneof six classes (1, 0%; 2, 10%; 3, 30%; 4, 50%; 5, 70%; 6,90%) in three subplots per stand. Cover of grass, vegeta-tion-free needle litter and the five most common forest floorbryophytes were visually estimated in all subplots sepa-
rately, that is, all ten 10 m � 10 m squares within the largeplot. In each subplot, we measured the height and cut-sur-face diameter of each stump (>10 cm) and the length anddiameter of each log (>10 cm), and calculated surface(mantel) area available for colonization (2/3 of the surfacearea of a cylinder for the logs and the cut stump area forthe stumps). Deadwood overgrown by forest floor bryo-phytes was not included. A list of all bryophyte species wascompiled for each subplot, making it possible to representthe occurrences of each species by a frequency value of 0–10 for each plot. In every subplot, we searched and recordedspecies occurrences for 10 min each. Samples of bryophytesthat could not be identified in the field were collected forlater identification using a light microscope. To ensure aneffective data collection, the species pairs Dicranum fusces-cens – flexicaule, Plagiothecium laetum – curvifolium, Chi-loschyphus pallescens – polyanthus, and Cephalozialunulifolia – affinis were treated as four separate taxa to-gether with Bryum sp., which we also considered as onetaxon. The nomenclature follows Hallingback et al. (2006).Prior to analyses the list of encountered species was dividedinto three guilds based on the literature (Hallingback 1996)and personal knowledge of the species: epigeic species (i.e.,growing on forest floor), epixylic species (i.e., growing ondeadwood), and epilitic species (growing on rock and bould-ers). All encountered species except two epiphytic species(Ulota crispa and Metzgeria furcata) were classified intothese three guilds (see Table A1).
Statistical analysisTo get a measure of species compositional differences
among stands, we performed a two-dimensional nonmetricmultidimensional scaling (NMDS) ordination (using Bray–Curtis distance measure on a matrix with species frequen-cies) on each guild. Bray–Curtis measure of distance waschosen, since it is regarded to be relatively insensitive tothe influence of rare species (McCune and Grace 2002).The magnitude of difference in ordination scores was inter-preted as the degree of compositional dissimilarity betweensites, so that sites with only slight differences in ordinationscore values were compositionally similar to each other. Wethen rotated each ordination so that the scores of the firstaxis were as much correlated as possible with forest age.The second axis thus represents other variation in the data,which we do not interpret in this study. The rotated sitescores were then used as response variables in our aim tosearch for patterns (that possibly could be nonlinear or evennonmonotonic) in species compositional changes over time.We used the robust, nonparametric regression method LO-ESS (locally weighted scatter plot smoothing) with a rela-tively narrow smoothing parameter (span, 0.5) that producesa smooth curve through a set of data points (see, e.g., Trex-ler and Travis 1993). The choice of the width of the smooth-ing parameter (how large a span of the data that should beused in each local computation) is somewhat subjective inLOESS regression. We chose a somewhat narrower widthcompared with the default settings in many statistical soft-wares, since our purpose with this study was to search forpatterns rather than to build models. To evaluate the robust-ness of the smoothed function, we plotted approximate 95%confidence bands calculated as two times the standard error
Fig. 1. Map of the study area in south-central Sweden with dots in-dicating the location of all 31 sampled stands.
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for the predicted values along the curve. For each LOESSregression, we also present an estimate of the effective de-grees of freedom telling something about the complexity ofthe function. Apart from the NMDS analyses, which wereconducted in PC-ORD (McCune and Mefford 1999), all stat-istical analyses were performed in R version 2.4.0 (R Devel-opment Core Team 2007).
Results
Environmental variablesBryophyte cover increased up to an asymptote of 85%
cover after approximately 40 years (Fig. 2A), coinciding intime with the highest values for canopy cover at around65%–70% (Fig. 2B). There was a large variation in grasscover in young stands, but the general trend was a declinein cover over time (Fig. 2C). No site had particularly highlitter cover (the highest value was 23.7%), and there was noclear relationship between litter cover and time since clear-cutting (Fig. 2D). Surface area of total CWD (logs andstumps pooled) was at the lowest at 30–40 years after clear-cutting (Fig. 2E), while large logs (>25 cm) basically wereabsent in the first 70–80 years (Fig. 2F).
Fig. 2. Change in (A) bryophyte cover (%); (B) canopy cover (%); (C) grass cover (%); (D) litter cover (%); (E) total coarse woody debris(CWD) area (m2); and (F) large log area (>25 cm) along a chronosequence of 31 spruce-dominated stands. A regression line was fittedusing LOESS (locally weighted scatterplot smoothing) with a smoothing parameter of 0.5. Downed logs were defined as ‘‘large logs’’ if thediameter exceeded 25 cm. Effective degrees of freedom: 23.3 (A), 23.9 (B), 23.4 (C), 23.9 (D), 23.7 (E), and 23.9 (F); 95% confidencebands were added to the line to facilitate the evaluation of the LOESS functions.
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Species compositionSpecies composition of the epigeic guild on the clearcuts
was clearly dissimilar to the late successional communitycomposition (Fig. 3A). We did not find any bottleneck phasewith retrogressive succession in any of the three guilds, butinstead the species composition gradually became more sim-ilar to older stands. After approximately 40 years, no majorchange in the species composition could be detected. Differ-ent forest floor species exhibited different patterns of recov-ery (e.g., earlier recovery of Pleurozium schreberi comparedwith Dicranum majus, Table A1, Fig. S1, Table S12). Thespecies composition in the epilitic guild was characterizedby considerable among-site variation in all ages (Fig. 3B).The species composition of epixylic species in the youngeststands was dissimilar to the composition in mature forests,and a considerable recovery was evident in this guild al-ready after 45–50 years (Fig. 3C). Interestingly, the speciescomposition in the mature stands seemed to become moresimilar to the younger stands along the rotated first ordina-tion axis (Fig. 3C).
DiscussionRecovery of forest understorey communities after clear-
cut logging is known to be a relatively slow process (Duffyand Meier 1992; Dynesius and Hylander 2007) potentiallylimited by factors such as substrate deficiency (Rambo andMuir 1998), unsuitable microclimate (Soderstrom 1988),and dispersal limitation (Soderstrom 1987). This study how-ever verifies that the clear-cutting (and perhaps the follow-ing years) is the most problematic phase for latesuccessional bryophytes during the rotation cycle in thestudied forest landscape. The general pattern obtained washence a monotonic increase in similarity towards the speciescomposition found in the later successional stages, with noother bottlenecks along the successional trajectory in youngand semi-mature forests.
We had hypothesized that high initial grass cover onclearcuts, high litter cover and canopy cover in semimatureforests might cause bottlenecks for the bryophyte commun-ities along the successional trajectory. More detailed studiesduring this period would be needed to sort out if the in-crease in grass cover after clear-cutting will increase or de-crease local extinction rates after clear-cutting. Quiteunexpected was the lack of a period of high litter or canopycover in young stands prior to the first thinning (Figs. 2B,2D). Apparently, the investigated stand type does not regu-larly develop dense stands without understory in this region.The possibility of a bottleneck during succession due todense stand conditions could, however, still be valid inother, perhaps more productive, regions (e.g., Rambo andMuir 1998).
An important question is to what degree systematic differ-ences in silvicultural methods during certain time periodsmight have affected our results. It is not unlikely that mostof the stands that now are 50–60 and 80–90 years old wereburnt directly after the clear-cutting (Lars Ostlund, personalcommunication 2009; Ostlund et al. 1997). Although resultsfrom previous studies suggest a higher initial loss of bryo-phytes after fire and a more pronounced grass dominanceafter logging, successional trajectories seem to converge atapproximately 30–40 years (Rees and Juday 2002; Uotilaand Kouki 2005). Our results do not indicate any special de-viation from the main pattern during this period, but if thispractice had been more recent it might have biased our in-terpretations. Another possible systematic problem is thatthe stands that now are 70–80 years old are likely to havebeen fertilized, since this practice was very common inyoung spruce stands in central Sweden between 1960 and1970 (Lars Ostlund, personal communication 2009; Ostlundet al. 1997). Since addition of N-fertilizers has been shownto affect bryophyte communities (e.g., negative effect onHylocomium splendes and positive on Brachythecium re-
Fig. 3. Change in species composition for (A) epigeic species; (B) epilitic species; and (C) epixylic species along a chronosequence of 31spruce-dominated stands. A regression line was fitted using LOESS (locally weighted scatterplot smoothing) with a smoothing parameter of0.5. For each guild, the temporal changes in ordination scores for the rotated first axis (from a two-dimensional NMDS ordination) areshown. The stress values for the ordinations were as follows: 15 (epigeics), 15.4 (epilitics), and 9.9 (epixylics). Effective degrees of free-dom: 23.9 (A), 22.9 (B), and 23 (C); 95% confidence bands were added to the line to facilitate the evaluation of the LOESS functions.
2 Supplementary data for this article are available on the journal Web site (http://cjfr.nrc.ca) or may be purchased from the Depository ofUnpublished Data, Document Delivery, CISTI, National Research Council Canada, Building M-55, 1200 Montreal Road, Ottawa, ON K1A0R6, Canada. DUD 5285. For more information on obtaining material refer to http://cisti-icist.nrc-cnrc.gc.ca/eng/ibp/cisti/collection/unpub-lished-data.html.
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flexum) up to 47 years after addition (Strengbom et al.2001), this can possibly have affected our results. However,since no deviation from the main pattern was found duringthis period, we feel sufficiently confident in the main resultsobtained from this chronosequence.
Forest floor bryophyte successionDuring canopy closure, the forest floor bryophyte succes-
sion displayed a gradual increase in compositional similaritytowards the old forest composition with pioneer species suchas Ceratodon purpureus and Polytrichum juniperinum beingreplaced by large mat-forming mosses (pleurocarps). Inter-estingly, the changes in abundance pattern of the most dom-inant forest floor species, for example, Pleuroziumschreberi, Hylocomium splendens, and Dicranum majus,were found to be substantial, even after the asymptotic totalforest floor bryophyte cover of around 85% had been at-tained. Competition among bryophytes is usually diffuseand mainly for space rather than growth-limiting resources(During and van Tooren 1990). In a boreal black spruce(Picea mariana) forest in northern Ontario, Frego and Carle-ton (1995) were unable to relate spatial abundance patternsamong the four most dominant forest floor species to varia-tion in microsite tolerance. In a following study, the domi-nant forest floor species Pleurozium schreberi was found tobe most successful in colonizing experimentally createdgaps, suggesting a role of regeneration strategy in structur-ing forest floor guilds (Frego 1996). It is likely that thishighly efficient lateral spread, in combination with its highability to withstand drought is responsible for the quicker re-covery seen in Pleurozium than in some other forest floorspecies.
Bryophyte succession on bouldersMany of the dominant species in the boulder guild are
drought resistant and could be found in semi-open habitatssuch as rocky outcrops, for example, Racomitrium microcar-pon and Hedwigia ciliata. Apparently, many of the epiliticspecies present in mature forests survive the clear-cuttingphase and seem to be indifferent to changes in light regimefollowing canopy closure (Fig. 3B).
Bryophyte succession on woody debrisInterestingly, we did not find a shortage of CWD to con-
strain the recovery of the epixylic bryophyte flora, as seenwhen comparing the curves for woody debris (Figs. 2E, 2F)and ordination scores (Fig. 3C). The change in epixylic spe-cies composition, during the first 50 years, was likely ex-plained by a gradual change towards a more favorablemicroclimate associated with canopy closure. Recolonizingspecies thus seem to be able to disperse and establish onthe small amount of woody debris that is available duringthis time period. Our results suggest that the species compo-sition of mature forests has already been reached at 50 yearsafter harvest, before the onset of any substantial accumula-tion of woody debris. These findings contrast with those ob-tained from stream-side forests in northern Sweden, wherespecies richness and abundance of bryophytes on convexsubstrates (including CWD) were substantially lower than inold-growth forests 30–50 years after clear-cutting (Dynesiusand Hylander 2007). This incongruence has certainly to do
with the different endpoints in the two studies — matureforests developing after clear-cutting in a heavily managedlandscape in our study and old-growth forests that still haveviable populations of many specialist species in the case ofDynesius and Hylander (2007). Most epixylic species in ourstudy have relatively broad substrate preferences (e.g., ableto utilize fine woody debris and other substrate types cov-ered by humus), and the few epixylic specialists encoun-tered, for example, Anastrophyllum hellerianum, Lophozialongiflora, and Herzogiella seligeri, are all very infrequentand restricted to the oldest stands (see Table A1). The lackof a clear response to increased substrate availability after50 years during the reassembly process might be related thelong history of intense forestry in the area, which mighthave reduced source populations of obligate epixylics withspecific substrate preferences. Interestingly, the species com-position of the epixylic guild in several mature standsshowed signs of retrogression and tended to be more similarin composition to younger stands (Fig. 3C). This pattern isdifficult to understand in the light of microsite limitation,since deadwood became more abundant (Figs. 2E, 2F). Onepossibility is that the difference in microclimate betweensomewhat denser semi-mature stands and mature stands thathave been thinned a second time is unfavorable for somecommon species that can utilize fine woody debris.
Conclusions and management implicationsSince we did not find any clearly defined bottleneck in
species composition during the succession after clear-cutlogging, our study suggests that efficient conservation meas-ures should continue to focus on alternative logging methodswith the aim of increasing the in situ survival. However, aswas evident for woody debris species, the recovery can beconstrained by factors other than the most apparent (e.g.,high recovery despite lack of substrate). An important ques-tion that needs further attention is to what extent additionalwoody debris during both pre- and post-thinning phasescould be utilized by late successional epixylic specialistsand to evaluate the relative importance of microclimaticconstrains and dispersal limitations in shaping the reassem-bly process.
AcknowledgementWe thank B. Pettersson and R. Andersson at the forest
companies Bergvik Skog AB and Sveaskog for providing uswith stand data and J. Loenberg for field assistance. Wethank O. Eriksson, L. Gustafsson, and P. Milberg for valua-ble comments on earlier versions of the manuscript. Thisstudy was supported by a grant from the Swedish ResearchCouncil to K.H..
ReferencesAhti, T., Hamet-Ahti, L., and Jalas, J. 1968. Vegetation zones and
their sections in Northwestern Europe. Ann. Bot. Fenn. 5: 169–211.
Baker, W.L., and Walford, G.M. 1995. Multiple stable states andmodels of riparian vegetation succession on the Animas River,Colorado. Ann. Assoc. Am. Geogr. 85(2): 320–338. doi:10.1111/j.1467-8306.1995.tb01797.x.
Belyea, L.R., and Lancaster, J. 1999. Assembly rules in within a
1876 Can. J. For. Res. Vol. 39, 2009
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. J. F
or. R
es. D
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d fr
om w
ww
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rese
arch
pres
s.co
m b
y U
OV
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For
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onal
use
onl
y.
contingent ecology. Oikos, 86(3): 402–416. doi:10.2307/3546646.
Bergstedt, J., and Milberg, P. 2001. The impact of logging intensityon field-layer vegetation in Swedish boreal forests. For. Ecol.Manage. 154(1–2): 105–115. doi:10.1016/S0378-1127(00)00642-3.
DeLuca, T.H., Zackrisson, O., Nilsson, M.C., and Sellstedt, A.2002. Quantifying nitrogen-fixation in feather moss carpets ofboreal forests. Nature (London), 419(6910): 917–920. doi:10.1038/nature01051. PMID:12410308.
Duffy, D.C., and Meier, A.J. 1992. Do Appalachian herbaceous un-derstories ever recover from clearcutting? Conserv. Biol. 6(2):196–201. doi:10.1046/j.1523-1739.1992.620196.x.
During, H.J., and van Tooren, B.F. 1990. Bryophyte interactionwith other plants. Bot. J. Linn. Soc. 104(1–3): 79–98. doi:10.1111/j.1095-8339.1990.tb02212.x.
Dynesius, M., and Hylander, K. 2007. Resilience of bryophytecommunities to clear-cutting of boreal stream-side forests. Biol.Conserv. 135(3): 423–434. doi:10.1016/j.biocon.2006.10.010.
Ekbom, B., Schroeder, M., and Larsson, S. 2006. Stand specific oc-currence of coarse woody debris in a managed boreal forestlandscape in central Sweden. For. Ecol. Manage. 221: 2–12.
Esseen, P.A., Ehnstrom, B., Ericson, L., and Sjoberg, K. 1997. Bor-eal forests. Ecol. Bull. 46: 16–47.
Fenton, N.J., Frego, K.A., and Sims, M.R. 2003. Changes in forestfloor bryophyte (moss and liverwort) communities 4 years afterforest harvest. Can. J. Bot. 81(7): 714–731. doi:10.1139/b03-063.
Freden, C. 1994. Ed. in Berg och jord. Svensk National Atlas(SNS), Stockholm.
Frego, K.A. 1996. Regeneration of four boreal bryophytes: coloni-zation of experimental gaps by naturally occurring propagules.Can. J. Bot. 74(12): 1937–1942. doi:10.1139/b96-231.
Frego, K.A., and Carleton, T.J. 1995. Microsite tolerance of fourbryophytes in a mature black spruce stand: reciprocal trans-plants. Bryologist, 98(4): 452–458. doi:10.2307/3243584.
Frelich, L.E., Calcote, R.R., Davis, M.B., and Pastor, J. 1993. Patchformation and maintenance in an old growth hemlock–hardwoodforest. Ecology, 74(2): 513–527. doi:10.2307/1939312.
Hagglund, B., and Lundmark, J.E. 1999. Bonitering-Markvegeta-tionstyper, Skogsmarksflora. Skogstyrelsens forlag, Jonkoping.
Hallingback, T. 1996. Ekologisk katalog over mossor. Artdataban-kens forlag [Swedish Species Information Center PublishingCenter], Uppsala, Sweden.
Hallingback, T., Hedenas, L., and Weibull, H. 2006. Ny checklistafor Sveriges mossor. Sven. Bot. Tidskr. 100: 96–148.
Hannerz, M., and Hanell, B. 1997. The effect of the flora in Nor-way spruce forest following clearcutting and shelterwood cut-ting. For. Ecol. Manage. 90(1): 29–49. doi:10.1016/S0378-1127(96)03858-3.
Hylander, K., Dynesius, M., Jonsson, B.G., and Nilsson, C. 2005.Substrate form determines the fate of bryophytes in riparian buf-fer strips. Ecol. Appl. 15(2): 674–688. doi:10.1890/04-0570.
Johansson, T. 1987. Irradiance in thinned Norway spruce (Piceaabies) stands and the possibility to prevent suckers of broad-leaved trees. For. Ecol. Manage. 20(3–4): 307–319. doi:10.1016/0378-1127(87)90087-9.
Keenan, R.J., and Kimmins, J.P. 1993. The ecological effects ofclear-cutting. Environ. Rev. 1: 121–144.
Kruys, N., Fries, C., Jonsson, B.G., Lamas, T., and Stahl, G. 1999.
Wood-inhabiting cryptogams on dead Norway spruce (Piceaabies) trees in managed Swedish boreal forests. Can. J. For.Res. 29(2): 178–186. doi:10.1139/cjfr-29-2-178.
McCune, B., and Grace, J.B. 2002. Analysis of ecological commu-nities. MjM Software Design, Gleneden Beach, Ore.
McCune, B., and Mefford, M.J. 1999. PC-ORD. Multivariate ana-lysis of ecological data. MjM Software Design, Gleneden Beach,Ore.
Nilsson, N.E. (Editor). 1996. Skogen. 2nd ed. Sveriges NationalAtlas (SNS), Stockholm.
Ostlund, L., Zackrisson, O., and Axelsson, A.-L. 1997. The historyand transformation of the Scandinavian boreal forest landscapesince the 19th century. Can. J. For. Res. 27: 1198–1206.
R Development Core Team. 2007. R: A language and environmentfor computing. R Foundations for Statistical Computing, Vienna,Austria.
Raab, B., and Vedin, H. (Editors). 1999. Klimat, sjoar och vatten-drag. Svensk National Atlas (SNS), Stockholm.
Rambo, T.R., and Muir, P. 1998. Forest floor bryophytes of Pseu-dotsuga menziesii–Tsuga heterophylla stands in Oregon: influ-ence of substrate and overstory. Bryologist, 101: 116–130.
Rees, D., and Juday, G.P. 2002. Plant species diversity on loggedversus burned sites in central Alaska. For. Ecol. Manage.155(1–3): 291–302. doi:10.1016/S0378-1127(01)00566-7.
Rosenvald, R., and Lohmus, A. 2008. For what, when and where isgreen-tree retention better than clear-cutting? A review of thebiodiversity aspects. For. Ecol. Manage. 255(1): 1–15. doi:10.1016/j.foreco.2007.09.016.
Schimmel, J., and Granstrom, A. 1996. Fire severity and vegetationresponse in the boreal Swedish forest. Ecology, 77(5): 1436–1450. doi:10.2307/2265541.
Soderstrom, L. 1987. Dispersal as a limiting factor for distributionamong epixylic bryophytes. Symp. Biol. Hung. 35: 475–483.
Soderstrom, L. 1988. The occurrence of epixylic bryophyte and li-chen species in an old natural and a managed forest stand innortheast Sweden. Biol. Conserv. 45(3): 169–178. doi:10.1016/0006-3207(88)90137-1.
Strengbom, J., Nordin, A., Nasholm, T., and Ericson, L. 2001.Slow recovery of boreal forest ecosystem following decreasednitrogen input. Funct. Ecol. 15(4): 451–457. doi:10.1046/j.0269-8463.2001.00538.x.
Trexler, J.C., and Travis, J. 1993. Nontraditional regression ana-lyses. Ecology, 74(6): 1629–1637. doi:10.2307/1939921.
Uotila, A., and Kouki, J. 2005. Understorey vegetation in spruce-dominated forests in eastern Finland and Russian Karelia: suc-cessional patterns after anthropogenic and natural disturbances.For. Ecol. Manage. 215(1–3): 113–137. doi:10.1016/j.foreco.2005.05.008.
Wardle, D.A., Walker, L.R., and Bardgett, R.D. 2004. Ecosystemproperties and forest decline in contrasting long-term chronose-quences. Science (Washington, D.C.), 305(5683): 509–513.doi:10.1126/science.1098778. PMID:15205475.
Whittaker, R.H. 1953. A consideration of climax theory: the climaxas a population and pattern. Ecol. Monogr. 23(1): 41–78. doi:10.2307/1943519.
Appendix AAppendix appears on the following page.
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Table A1. Species list showing taxonomic affiliation, total number of plot occurrences, and mean plot frequency (%)of species in the three guilds; epigeic (forest floor species), epilitic (boulder living species), and epixylics (deadwoodliving species) over time divided into three age-classes: 2–12, 20–65, and 66–96 years after clear-cutting.
Mean plot frequency (%)
Total no. of stands,n = 31
2–12 years(%), n = 10
20–65 years(%), n = 14
66–96 years(%), n = 7
Epigeic speciesMosses
Atrichum undulatum 10 20 0.8 7.1Aulacomnium palustre 21 17 24.3 17.1Brachythecium rutabulum 25 22 36.7 27Calliergon cordifolium 1 0 0.7 0Ceratodon purpureus 9 74.4 3.5 0Cirriphyllum piliferum 1 0 2.8 0Dicranella heteromalla 3 8 0 2.8Dicranum drummondi 2 2.2 0 1.4Dicranum majus 28 28 84 97Dicranum polysteum 31 97 92 98Dicranum scoparium 31 95 100 98Dicranum spurium 1 5 0 0Ditrichum heteromallum 5 5 0.7 1.4Ditrichum pusillum 3 4 0 0Eurhynchium angustirete 1 0 0.7 0Herzogiella striatella 1 1 0 0Hylocomium splendens 30 79 100 85Hylocomiastrum umbratum 2 0 0.7 7.1Mnium hornum 1 0 0 1.4Plagiomnium affine 8 8 15 6.2Plagiothecium undulatum 2 0 0 2.8Pleurozium schreberi 31 100 100 100Pogonatum nanum 3 3 0 0Pogonatum urnigerum 7 26 0 1.4Pohlia cruda 1 0 0 2.8Pohlia nutans 31 95 85 85Polytrichum commune 22 58 21 34Polytrichastrum formosum 20 39 19 30Polytrichum juniperinum 19 84 10 16Pseudotaxiphyllum elegans 5 3 2 3Psudephemerum nitidum 2 2 0 0Ptilium crista-castrensis 25 21 60 88Rhizomnium punctatum 2 0 2.1 0Rhodobruym roseum 3 8 7 0Rhytidiadelphus squarrosus 1 0 0.7 0Rhytidiadelphus subpinnatus 1 0 0.7 0Rhytidiadelphus triquetrus 3 0 3 1.5Schistostega pennata 1 0 0 1.4Sciuro-hypnum oedipodium 25 26 50 28Sciuro-hypnum starkei 10 6 10 8Sphagnum angustifolium 6 0 8 1.5Sphagnum capillifolium 12 15 13 11.5Sphagnum girgensohni 27 23 65 60Sphagnum quinquefarium 3 0 6 0Sphagnum squarrosum 3 1.1 1.5 0Splachnum luteum 3 0 1.8 1.3Splachnum rubrum 4 2.2 3.6 0Thuidium tamariscinum 1 0 0.7 0
LiverwortsBarbilophozia floerkii 9 0 7 12Barbilophozia lycopodioides 10 1.1 7.3 10
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Table A1 (continued).
Mean plot frequency (%)
Total no. of stands,n = 31
2–12 years(%), n = 10
20–65 years(%), n = 14
66–96 years(%), n = 7
Blasia pusilla 1 1 0 0Calypogeia mulleriana 13 2 7 10Cephalozia bicuspidata 24 17 20 24Cephaloziella divaricata 1 0 0.7 0Chiloschyphus pallescens –
polyanthos1 1.4 1.8 0
Diplophyllum obtusifolium 4 9 0 0Jungermannia caespiticia 2 2 0 0Jungermannia gracillima 1 1 0 0Lophozia bicrenata 2 1 0.7 0Lophozia obtusa 9 2 10 4Nardia scalaris 4 7 0.7 1.4Pellia epiphylla 1 0 1.4 0Plagiochila asplenoides 9 1 21 13Ptilidium ciliare 26 21 24 41Scapania curta 1 1 0 0Scapania umbrosa 2 1 0 1.4Scapania sp. 1 0 0.7 0
Epilitic speciesMosses
Andreaea rupestris 29 42 37 48Cynodontium strumiferum 12 5 5 15Grimmia muehlenbecki 1 0 0 1.5Hedwigia ciliata 10 5 4 22Isothecium myosuroides 5 6 0.8 1.25Kiaera blytti 2 1 0 2.5Paraleucobryum longifolium 26 32 32 46.3Plagiothecium denticulatum 29 52 70 81.3Racomitrium fasciculare 1 0 0 1.25Racomitrium heterostichum 18 20 6 8Racomitrium lanuginosum 2 0 0 2.5Racomitrium microcarpon 17 9 22 16
LiverwortsAnastrophyllum minutum 8 1 3 7Barbilophozia barbata 7 5 2 6Barbilophozia hatcheri 9 1 3 11Diplophyllum taxifolium 1 0 0 1.25Scapania nemorea 4 0 2.3 1.25Tritomaria quinquedentata 7 1 5 2.5
Epixylic speciesMosses
Aulacomnium androgynum 1 0 0 1.4Brachythecium velutinum 5 3 3 4Dicranum fuscescens –
flexicaule31 83.3 90 93.8
Dicranum montanum 19 14 12 17Herzogiella seligeri 6 1.1 1.5 7Plagiothecium laetum –
curvifolium30 47.7 93 87
Tetraphis pellucida 30 41 79 95Liverworts
Anastrophyllum hellerianum 1 0 0 1.5Anastrophyllum michauxii 1 0 0 1.5Barbilophozia attenuata 28 34.4 74.5 76.3Blepharostoma trichophyllum 26 15 60 48
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Table A1 (concluded).
Mean plot frequency (%)
Total no. of stands,n = 31
2–12 years(%), n = 10
20–65 years(%), n = 14
66–96 years(%), n = 7
Calypogeia integristipula 24 8 72 78Cephalozia lunulifolia –
affinis23 4.4 35 17
Lepidozia reptans 25 12 63 70Lophocolea heterophylla 22 16 51 41Lophozia longiflora 3 0 2.1 1.4Lophozia ventricosa. silvicola 26 22 47 55Ptilidium pulcherrimum 31 70 87 98Riccardia latifrons 3 0 2.8 0
Note: Mean plot frequency for each species was calculated as the total frequency divided with the total number of stands ineach age-class, i.e., frequency values of 50% meaning an average occurrence of 5 of 10 subplots within the large 0.1 ha plots forthat age-class.
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