An analysis of sucker regeneration of trembling aspen

REVIEW / SYNTHÈSE

An analysis of sucker regeneration of tremblingaspen

Brent R. Frey, Victor J. Lieffers, Simon M. Landhäusser, Phil G. Comeau,and Ken J. Greenway

Abstract: Aspen (Populus tremuloides Michx.) is a clonal tree species that commonly regenerates via root suckeringafter disturbance. This paper reviews the literature and identifies critical gaps in our understanding of the dynamics ofaspen root suckering. The role of plant growth regulators (e.g., hormones, carbohydrates), environmental conditions(e.g., soil moisture, temperature, nutrient availability), overstory disturbance (e.g., harvesting, wildfire), ground distur-bance (e.g., soil compaction, wounding or severing of roots), vegetation competition, predisturbance stand condition,and clonal (genetic) differences are discussed as they relate to sucker initiation, sucker growth, and (or) patterns of siteestablishment. The paper presents a series of conceptual figures summarizing our knowledge of the factors controllingsuckering dynamics and identifies areas of future research.

Résumé : Le peuplier faux-tremble (Populus tremuloides Michx.) est une espèce clonale qui se régénère généralementpar drageonnement racinaire après une perturbation. Cet article passe en revue la littérature et identifie les points criti-ques qui font défaut dans notre compréhension de la dynamique du drageonnement racinaire chez le peuplier faux-tremble. Le rôle des régulateurs de croissance (p. ex. hormones, hydrates de carbone), les conditions environnementales(p. ex. humidité du sol, température, disponibilité des nutriments), la perturbation du couvert (p. ex. récolte, feux de fo-rêt), la perturbation du sol (p. ex. compaction du sol, bris ou dommages aux racines), la végétation compétitrice, lescaractéristiques du peuplement antérieurement à une perturbation et les variations clonales (génétiques) sont abordés enlien avec l’initiation et la croissance des drageons et les patrons d’établissement sur un site. L’article contient une sériede schémas conceptuels qui résument nos connaissances à propos des facteurs qui contrôlent la dynamique du drageon-nement et identifient les préoccupations futures de recherche.

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Introduction

Aspen (Populus tremuloides Michx.) is a clonal tree spe-cies that commonly regenerates via root suckering after dis-turbance removes or kills the aboveground portions of theclone. Abundant root suckering is thought to be importantfor ensuring the successful reestablishment of vigorous as-pen stands after disturbance. On the other hand, vigorous as-pen suckering can pose competition problems for othercommercially important tree species. An improved under-standing of the factors that control aspen suckering will ben-efit both management efforts aimed at promoting aspenestablishment and, conversely, efforts aimed at limiting itsregeneration to reduce competitive effects on other tree spe-

cies. Although reviews of the physiology of root suckering(Schier 1981) and regeneration dynamics (Schier et al. 1985;Doucet 1989; Navratil 1991) have been undertaken in thepast, these have been limited in focus. Furthermore, recentfindings related to environmental effects on sucker initiationand the importance of the clonal root system to sucker den-sity and growth, in combination with ongoing uncertaintiesabout management impacts, suggest that revisiting the topicis warranted. This paper reviews the literature, highlightingnew knowledge and identifying critical gaps in our under-standing of the physiology and regeneration dynamics of as-pen root suckering. The primary geographic focus of thepaper is on suckering dynamics in North American borealmixedwood forests; however, we make use of information

Can. J. For. Res. 33: 1169–1179 (2003) doi: 10.1139/X03-053 © 2003 NRC Canada

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Received 29 May 2002. Accepted 5 February 2003. Published on the NRC Research Press Web site at http://cjfr.nrc.ca on26 May 2003.

B.R. Frey,1 V.J. Lieffers, S.M. Landhäusser, and P.G. Comeau. Centre for Enhanced Forest Management, Department ofRenewable Resources, University of Alberta, 4-42 Earth Sciences Building, Edmonton, AB T6G 2H1, Canada.K.J. Greenway. Alberta Research Council Inc., Bag 4000, Vegreville, AB T9C 1T4, Canada.

1Corresponding author (e-mail: [email protected]).

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obtained from studies throughout its North American geo-graphic range.2

Physiological and environmental factorsinfluencing sucker initiation (Fig. 1)

Physiological processes of sucker initiationRoot suckers originate from primordia that are formed

from meristematic cells during secondary growth in the corkcambium of the roots (Schier 1973a; Schier et al. 1985).Sucker primordia are abundant and can be present in differ-ent developmental stages as primordia, fully developed sup-pressed buds, or short shoots (Brown 1935; Sandberg 1951;Schier 1973a). However, newly initiated meristems and pre-existing primordia, rather than suppressed buds or shortshoots, are responsible for most suckering after disturbance(Sandberg 1951; Schier 1973a). Indeed, the growth of suck-ers arising from suppressed buds tends to be much less vig-orous than that of the other two sources (Sandberg 1951;Schier 1973a). Two- to four-fold differences in abundance ofprimordia have been observed among clones; thus clonal dif-ferences contribute substantially to the observed variation insucker initiation among sites (Zasada and Schier 1973). It isnot clear, however, to what extent nongenetic factors (e.g.,site factors, physiological condition of the root) affect thedensity of primordia and the number of suckers that initiate.

Sucker initiation in aspen is inhibited by apical dominance(Farmer 1962; Eliasson 1971a; Schier 1972; Steneker 1974),a condition that is primarily thought to be mediated by the

activity of the hormones auxin and cytokinin. Auxin is pro-duced in aboveground tissues (mostly twigs and buds) and istransported in the phloem to the roots, inhibiting sucker budinitiation (Eliasson 1971a; Schier 1972) and promoting rootgrowth (Hicks 1972). Cytokinins, in contrast, are producedin actively growing root tips, exhibit polar movement awayfrom the root tips towards the stem (opposite to auxin), andare known to play an important role in the initiation of shootdevelopment on roots in many plants (Peterson 1975;Thimann 1977) by counteracting the activity of auxin (Hicks1972).

Most physiological studies of aspen sucker initiation havefocused on a direct role for auxin in the maintenance of api-cal dominance. Farmer (1962) and Schier (1981) demon-strated that sucker initiation is reduced on root cuttingstreated with auxin, or stimulated by applying auxin inhibi-tors such as α-(p-chlorophenoxy)isobutyric acid (Schier1975a). Apical dominance can be disrupted by treatmentsthat interrupt auxin transport between the shoot and the rootsystem, such as stem girdling or root severing (Farmer1962), or by disturbances that limit auxin production, suchas stem removal (Eliasson 1971a; Schier 1972) and perhapsdefoliation (Schier 1975b). Furthermore, the ability of rootsegments to initiate suckers is negatively correlated with sea-sonal increases in root auxin levels (Schier 1973b).

While acknowledging an important role for auxin in api-cal dominance, it must be stated that a direct role for auxinin the apical dominance of plants is largely refuted in thewider plant physiology literature (e.g., Wareing and Philips1979). Rather, auxin is considered to operate indirectly,likely through its interactions with other hormones. Work onapical dominance in pea plants suggests that auxin may op-erate indirectly by promoting an increase in ethylene synthe-sis (Ahmad et al. 1987), which then inhibits bud outgrowth(Blake et al. 1984; Yeang and Hillman 1984). Alternatively,auxin may direct the transport of cytokinins to meristems,which then determine whether buds initiate (Wareing andPhilips 1979). However, studies in other plants (e.g., inAribidopsis, Chatfield et al. 2000) have not found strong evi-dence for the involvement of other growth regulators such asabscisic acid, ethylene, or cytokinin in the inhibition ofbuds. Regardless, continuing questions about the physiologi-cal mechanisms of apical dominance in other plants stronglyargue for further investigation into the growth regulators in-volved in the apical dominance of aspen.

The release of buds from apical dominance is primarilyattributed to the activity of cytokinins. Increased levels ofcytokinins, for example, have been shown to stimulate shootinitiation in aspen tissue cultures (Winton 1968; Wolter1968). Schier (1981) demonstrated that increasing thecytokinin/auxin ratio by the application of the cytokinin 6-benzylamina-purine (BAP) to roots increased the number ofsuckers initiated. However, other experiments by Schier(1981), using various natural and synthetic cytokinins, eitherfailed to promote or even decreased suckering. Furthermore,there have been no studies that have directly measuredcytokinin production or transport in aspen root systems, es-pecially after apical dominance had been disrupted. Indeed,

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Fig. 1. Factors affecting sucker initiation. Arrow thickness indi-cates the magnitude of the effect, broken lines indicate a nega-tive effect, question marks indicate the uncertain contribution ofthat factor, and arrows running through the highlighted “hor-mones” band indicate that those factors may directly influencesucker initiation or may be mediated by the activity of hor-mones.

2 This paper also includes findings from the work of Eliasson (1971a, 1971b, 1971c) on European aspen (Populus tremula L.), as it is a veryclosely related species to Populus tremuloides. Where appropriate, we also refer to other aspen species.

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little is known about either the seasonal dynamics of aspenfine roots (the sites of cytokinin production) or potential rootdieback after disturbance. The role of cytokinins in sucker-ing may therefore have been overstated given available evi-dence, suggesting further research into its production andactivity is required.

It is not clear how quickly apical dominance is reestab-lished after disturbance. Growing suckers produce auxin,even at the very earliest stages of development (Eliasson1971b; Schier 1972). Schier (1972) found that removal ofnewly initiated suckers from root sections resulted in agreater number of suckers initiating than without removal,suggesting apical dominance was exerted by newly sproutedsuckers. Eliasson (1971c), in contrast, found that the earliestdeveloping suckers did not appear to inhibit the initiation ofother suckers at the base of growing shoots. Eliasson(1971c) speculated that a number of factors, including highcytokinin levels, the polar transport of auxin away frombuds, or the inactivation of auxin, could limit the activity ofinhibitors produced by newly sprouting suckers, thereby de-laying the establishment of apical dominance. Further physi-ological studies investigating hormonal transport and activityin newly initiated suckers may help to resolve this apparentambiguity regarding the timing of reestablishment of apicaldominance.

Other growth regulators, such as abscisic acid (ABA) andgibberellic acid, may be involved in aspen suckering. Bothgrowth regulators have received less attention as potentialregulators of suckering, and their role is less clear (Schier1981). ABA is known to be an important inhibitor of suckerdevelopment (Schier et al. 1985), ensuring that sucker budsdo not flush until the following spring on trees disturbedlater in the season (Schier 1973c). Gibberellic acid is impor-tant for promoting bud flush and sucker elongation once api-cal dominance is removed, but high levels can inhibit thedevelopment of primordia (Schier 1973c).

Differences in carbohydrate levels, nutrient status, orother growth-contributing resources within the root such aslipid concentrations could also affect the number of suckersthat initiate. Despite the dependence of suckers on root car-bohydrate reserves until they reach the soil surface (Schierand Zasada 1973), Tew (1970), Schier and Zasada (1973),and Fraser et al. (2002) found no relationship between car-bohydrate levels and number of suckers initiated. In anotherstudy, Schier (1981) found no relationship between either ni-trogen or storage lipid concentrations and suckering. Conse-quently, there is no current data available to suggestrelationships between storage reserves and sucker numbers.

Environmental controls on sucker initiationHigher soil temperatures following disturbance have long

been considered the most important environmental factorcontrolling sucker initiation. High root temperatures havebeen thought to facilitate auxin degradation (Schier et al.1985; Hungerford 1988), and promote root growth andcytokinin synthesis (Williams 1972, cited in Hungerford1988) and thereby stimulate sucker initiation. A number ofgrowth chamber studies (Horton and Maini 1964; Maini andHorton 1966a; Gifford 1967; Zasada and Schier 1973) ob-served increasing numbers of suckers on root segments withincreasing root temperatures, up to a maximum temperature

of approximately 30°C. However, the short duration ofearlier studies and (or) their use of short root segments prob-ably unfairly biased sucker initiation to the higher tempera-ture treatments (Fraser et al. 2002). A recent study showedthat root segments from northern clones exposed to 12 to20°C (maximum soil temperatures typically occurring dur-ing suckering) had similar rates of sucker initiation whensubjected to the same number of degree-days (Fraser et al.2002). These results suggest that higher temperatures do notenhance total sucker initiation. Higher soil temperatures,however, do stimulate earlier initiation of suckers (Mainiand Horton 1966a; Zasada and Schier 1973; Fraser et al.2002), which will in turn provide a longer growing seasonfor suckers initiated at an earlier time. Consequently,warmer temperatures may contribute to improved sucker es-tablishment more by improving growth and survival, than byenhancing total sucker initiation (refer to Sucker growth sec-tion). Still, soil temperatures below the 12°C tested by Fra-ser et al. (2002) can be observed in midsummer in borealmixedwood stands (Hogg and Lieffers 1991), suggestingthat effects of colder soil temperatures (below 12°C) shouldbe investigated.

Other potential environmental cues for suckering, such asnutrient availability, soil pH, or soil moisture, have receivedsignificantly less attention. It is reasonable to hypothesizethat vigorous aspen suckering typically observed followingfire (Bartos and Mueggler 1981; Brown and DeByle 1987)could be stimulated by the increases in nutrient availabilityand (or) pH that follow burning (Feller 1982; Van Cleve andDyrness 1983). The effects of pH on sucker initiation havenot been studied, while the role of external nutrient avail-ability has received only limited attention. Fraser et al.(2002) fertilized root sections with CaSO4 and NH4NO3 andfound that sucker initiation was not enhanced. Nonetheless,further studies using intact root systems and a broader rangeof nutrients will likely be necessary to determine whethernutrient availability affects sucker initiation.

Though our understanding of the influence of soil mois-ture on sucker initiation is somewhat limited, soil moistureappears to influence suckering. Very dry or water-saturatedgrowing mediums reduce sucker initiation on root cuttings(Maini and Horton 1964; Schier et al. 1985), and flooding orwaterlogging after disturbance inhibits root suckering (Bateset al. 1990, cited in Peterson and Peterson 1995). The reduc-tion in site transpiration following logging, coupled withhigh precipitation, may result in high soil moisture condi-tions that impair suckering (Crouch 1986). Sucker establish-ment under wet conditions is likely limited by poor suckerinitiation (presumably because of poor oxygen availability)but may also be driven by increased root death and decay(S.M. Landhäusser, V.J. Lieffers, U. Silins, and W. Liu, un-published data). Given this possible important role of soilmoisture on sucker initiation, wet or dry soil moisture condi-tions at the time of suckering may alter the degree of suckerinitiation. This is likely one of the factors clouding our un-derstanding of the suckering potential of different ecosites.The yearly differences in precipitation prior to the normaltime of suckering may be as important to sucker initiation asthe general moisture class used to describe the ecosite. Inaddition, as there are likely to be differences in root damageor soil compaction related to logging under different soil

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moisture conditions, the effect of this damage is also con-founded with site conditions.

Factors influencing sucker growth andsucker stand dynamics (Fig. 2)

Sucker growthTemperature is an important determinant of early sucker

development. Higher soil temperatures stimulate earlier initi-ation of suckers (Maini and Horton 1966a; Zasada andSchier 1973; Fraser et al. 2002) and thereby promote earlieremergence of suckers through the soil surface (Zasada andSchier 1973). Cold soil temperatures, in contrast, signifi-cantly reduce juvenile growth in aspen (i.e., height, diame-ter, biomass) (Gifford 1967; Landhäusser and Lieffers 1998),likely because cold temperatures limit water uptake by roots(Wan et al. 1999). By mediating early growth, temperaturemay affect the competitive ability of emerging suckers andthus potentially affect sucker survival, thereby suggesting anindirect role of temperature on suckering (Fraser et al.2002).

Though root carbohydrates reserves do not influencesucker initiation, they are important to sucker growth earlyin development when the photosystem is not fully func-tional. Sucker growth is strongly correlated with totalnonstructural carbohydrates (TNC) of roots (Schier andZasada 1973; Landhäusser and Lieffers 2002), which candiffer both within a clone and among clones (Schier andJohnston 1971). Sucker growth is more limited on small rootsegments, apparently because of the limited availability ofTNC reserves (Steneker and Walters 1971). Additionally,Landhäusser and Lieffers (2002) observed that fall-cut sap-lings produce suckers with greater height growth, biomassproduction, and leaf area development compared withspring-cut saplings, an effect attributed to substantiallyhigher root TNC levels in the fall-cut saplings.

The role of nutrient availability in the early growth of as-pen has not been well investigated, especially consideringthat regeneration of aspen after wildfire is associated withdramatic increases in nutrient availability. Calcium has re-ceived the most attention, as it is of noted importance to as-pen (Alban 1982) and increases in availability afterdisturbance (Feller 1982; Frey 2001). Growth of young as-pen seedlings has been shown to improve with increased lev-els of available Ca, and Ca deficiency may be a primarycause of reduced growth (Lu and Sucoff 2001). Fertilizationof root cuttings with NH4NO3 and CaSO4 stimulated greatersucker growth in the very early stages (Fraser et al. 2002),although it was not clear whether the improved growth re-sponse was attributable to a more rapid emergence of thesprout through the growing medium, or to enhancedphotosynthetic activity in the first few days after emergenceabove the soil surface. Light surface fires have been shownto increase foliage nutrient concentration in mature aspenstands (James and Smith 1977) and in the first 3 years aftersuckering (Weber 1990). It is likely that this increase in fo-liar nutrient status stimulated higher photosynthetic rates andgrowth; however, few studies have linked growth in youngsucker stands to nutrient availability. King et al. (1999)noted a 65% increase in photosynthesis and 37% increase ingrowth when aspen seedlings were fertilized with N; how-ever, this only occurred in association with elevated soiltemperatures. As with temperature, nutrient availability mayaffect the competitive ability of emerging suckers by mediat-ing early growth and survival of suckers. This suggests a po-tential indirect role of nutrient availability on the numbers ofsuckers established after a disturbance (Fraser et al. 2002).

While soil temperature, carbohydrates, and nutrientsclearly affect growth, light availability is also critical. Lowlight intensities have been shown to diminish growth of ju-venile aspen (Farmer 1963; Gifford 1967); hence the highestrates of sucker growth are typically associated with distur-bances that kill and remove the entire overstory (Stoeckler

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Fig. 2. Factors affecting sucker growth. Arrow thickness indicates the magnitude of the effect, broken lines indicate a negative effect,and question marks indicate the uncertain contribution of that factor.

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and Macon 1956; Huffman et al. 1999). Low rates of growthassociated with disturbances that retain part of the aspenoverstory, however, are likely not entirely a function of re-duced light conditions and lower rates of photosynthesis.The low photosynthetic light compensation point measuredon aspen seedlings indicates that a positive carbon balanceunder low light conditions could be sustained, given noother constraining factors (Landhäusser and Lieffers 2001).However, given the preferential allocation of C to the rootsystem in aspen grown under shade (Landhäusser andLieffers 2001, 2002), top growth is reduced. Apical control(sensu Zimmerman and Brown 1971) by the remainingoverstory and competition from dominant stems for theclonal resources may also constrain growth of suckers.

Competition may significantly impact aspen growth, de-pending on the site. On rich, moist sites, vigorous competi-tors, such as the grass Calamagrostis canadensis (Michx.)Beauv., can significantly reduce the growth of young aspen(Landhäusser and Lieffers 1998). Growth reductions arelikely, in part, attributable to increased competition for re-sources, but more importantly to low soil temperature condi-tions that are the result of the thick insulating litter ofcompetitors like C. canadensis (Hogg and Lieffers 1991;Landhäusser and Lieffers 1998). Landhäusser and Lieffers(1998) also suggested that the litter of such competitors maydiminish growth, possibly through allelopathic effects. Com-petitive ability of aspen suckers may also play a role in af-fecting the number of suckers that establish by interactingwith other environmental conditions. For example, tempera-ture or nutrient availability, by mediating early growth, mayaffect the competitive ability of emerging suckers andthereby affect sucker survival.

Early dynamics of sucker standsSucker densities typically peak in the first year after dis-

turbance then rapidly decline in the subsequent years, al-though sometimes substantial suckering may occur in thesecond year as well (Schier and Campbell 1978). First-yeardensities vary widely by region, sometimes exceeding250 000 stems/ha in the north-central U.S. (Alban et al.1994) where suckering is most vigorous, but densities aregenerally lower in the western U.S. and boreal mixedwoodof Canada (Steneker 1976; Bella 1986; Peterson and Peter-son 1992). High-density stands thin to ca. 20 000 stems/haby year 6 (Peterson and Peterson 1992); however, thinningmay not be evident in stands establishing at lower densities(e.g., Hendrickson 1988). Aspen regeneration often occurs inclumps of multiple stems (Shepperd 1993a), and clumpshave been observed to thin to a single stem by year 5(Sandberg 1951). Clumps are typically characterized by hav-ing a dominant stem with numerous subordinates (Shepperd1993a), and thinning is attributed to the loss of the smallersuppressed stems (Pollard 1971). Self-thinning of subordi-nates is likely driven by light competition (Shepperd 1993a).It is also speculated that the clonal connections increasecompetition for nutrients or carbohydrates or facilitate apicaldominance thereby accelerating the self-thinning process(Krasny and Johnson 1992), although source–sink relation-ships in aspen are not well understood. Vegetation competi-tion could contribute to the thinning process by reducinglight availability and soil temperatures, thereby limiting

sucker growth and establishment (Landhäusser and Lieffers1998). Wildlife browsing, especially in the western U.S.,may also contribute to sucker mortality and density reduc-tions, as aspen is a preferred browse species of wildlife(Smith et al. 2000; Peterson and Peterson 1992). The aspenshoot blight, Venturia macularis ((Fr.) Müll. & Arx.), is animportant pathogen in young sucker stands, damaging orkilling terminals and, in extreme cases, causing severe re-duction in height growth in some stands (Peterson and Peter-son 1992). Defoliating insects may also contribute tomortality and density reductions; however, there is little lit-erature on impacts of insects on young aspen sucker stands.

It is often assumed that initial sucker density is not criticalfor stand establishment given that juvenile stands of a rangeof stem densities converge to a common density (Petersonand Peterson 1992). This deserves further examination.Higher initial densities or greater leaf area has been shownto maintain more of the clonal root system (DesRochers andLieffers 2001a; Landhäusser and Lieffers 2002). Also, therapid development of leaf area in high density stands (Pinnoet al. 2001; Lieffers et al. 2002) should limit the encroach-ment of competing vegetation (Landhäusser and Lieffers1998). Several studies have shown that suckers that estab-lished at higher densities, and thus higher leaf areas, havehigher rates of growth and biomass production (Shepperd1993a; DesRochers and Lieffers 2001a; Landhäusser andLieffers 2002). Thus while stands may self thin, there appearto be benefits to sucker growth associated with high initialdensities. Furthermore, higher densities may ensure a moreuniform distribution and site capture, and provide insuranceagainst losses to browsing, pathogens, and insects (Petersonand Peterson 1992). Nonetheless, extremely high stem densi-ties have, in a few cases, been associated with reduced standgrowth of young sucker stands (Stone and Elliof 1998;Kabzems 2000) on severely disturbed sites. However, it ispossible that the observed reductions in growth in thesestudies were attributable to the negative effects of the severedisturbance and removal of organic layers from the siterather than the density.

Site, stand, and management factorsinfluencing regeneration (Fig. 3)

Effects of root distribution and stand condition onsuckering

The distribution of roots will to a large degree affectsucker establishment by determining the environment forsucker initiation and the susceptibility of roots to distur-bance. The smaller lateral roots (less than 2 cm in diameter)that produce most suckers (Kemperman 1978; Schier andCampbell 1978; DesRochers and Lieffers 2001a) are gener-ally dispersed at depths of 5–20 cm (Strong and LaRoi1983), although deeper rooting is evident in coarse-texturedsoils (Gifford 1966; Strong and LaRoi 1983). Most suckersoriginate from those lateral roots that are closest to the sur-face; in northern Ontario, 80–90% of suckers originatedfrom roots in the upper 5.9 cm and the remainder fromdepths of 10–12 cm (Kemperman 1978), while in Utah mostsuckers originated from the upper 15 cm (Schier and Camp-bell 1978). Nonetheless, deeper roots will sucker prolifically

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when a disturbance such as fire removes the forest floor cov-ering the roots (Brown and DeByle 1987).

This pattern has been thought to reflect a decline in suckerinitiation with depth, controlled by soil temperature. Basedon the findings of Fraser et al. (2002), temperature differ-ences (at least between 12–20°C) would not explain differ-ences in sucker initiation with depth in northern clones.Sucker initiation, however, might diminish substantially atdepths because temperatures might be cooler than 12°C. Itcould also be hypothesized that suckering is equally frequenton roots at deeper depths, but suckers initiated from deeperroots are less likely to become established because growthmay be slower as a result of cooler temperatures; carbohy-drates may be insufficient for emergence above the soil sur-face; development may be halted because of reestablishmentof apical dominance by suckers from more shallow roots;and (or) their late emergence may put them at a competitivedisadvantage relative to suckers developing from roots closerto the surface. Because most field studies measure suckernumbers above ground and later in the growing season, theremay be more sucker initiation (but not necessarily sucker es-tablishment) from deep roots than previously thought.

Site and stand conditions will likely interact to affect den-sity and distribution of suckers, and thus site capture, fol-lowing stand disturbance. Higher sucker densities arecorrelated with increasing preharvest basal area (Graham etal. 1963) and site index (Stoeckler and Macon 1956), pre-sumably in large part because of higher densities of roots inthe mature stand. However, the roots of more vigorous aspenclones have also been shown to produce higher numbers ofsuckers (Tew 1970). This suggests either an effect of nutri-ent availability or perhaps a genetic predisposition to greaternumber of suckers by clones growing on better (more com-petitive) sites, hence the linkage to site index. Regardless,there is almost certainly greater potential for suckering whenthe parental stands had higher basal area. For this reason weare uncertain about the generality of findings by Lavertu etal. (1994), who found that sucker density did not differacross a range of stands varying in preharvest basal area of 5

to 40 m2. However, this finding might be attributable to thelow experimental power of their study. Indeed, stands withlower basal area, such as decadent stands undergoingbreakup, are characterized by lower root densities and re-duced sucker establishment (Schier 1975b; Shepperd et al.2001). Poor sucker regeneration in some stands does not ap-pear to be limited by root age, as roots of older stands areequally capable of producing vigorous growing suckers(Schier and Campbell 1980). Instead, root distribution islikely the primary reason for the high variability in sucker-ing that is noted across regenerating sites (Shepperd 1993a).For example, Schier (1975b) noted that suckering occurredclosest to the living residual trees in stands that are breakingup, likely because root dieback in other areas created zonesof low root density. The development of vigorous under-stories in lower density stands or stands undergoing breakup(Schier and Campbell 1980; Shields and Bockheim 1981)may also limit sucker establishment. However, while it hasbeen acknowledged that both distribution and basal area –density of trees will affect the density of suckering across asite (Doucet 1989; Peterson and Peterson 1992), no studiesappear to have quantified spatial variability in suckering rel-ative to the distribution of trees. On northern mixedwoodsites the common occurrence of many small clones per hect-are (Steneker 1973), in combination with large clonal differ-ences in suckering (Peterson and Peterson 1992), likelycontributes to variation in sucker density across larger sites.Furthermore, areas of poor sucker regeneration within a sitemay also be ascribed to soil compaction and wounding dam-age to roots caused by machine traffic during harvesting(Bates et al. 1989; Navratil et al. 1991), which is addressedbelow.

Harvesting and traffic effectsThe number of mature aspen trees retained after logging

has been found to have a significant impact on the numberof suckers formed (Zehngraff 1947; Stoeckler and Macon1956; Maini and Horton 1966a; Schier and Smith 1979;Schier et al. 1985). Since ramets of a clone are typically inter-

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Fig. 3. Factors affecting sucker regeneration across a site after disturbance. Arrow thickness indicates the magnitude of the effect, bro-ken lines indicate a negative effect, and question marks indicate the uncertain contribution of that factor. LAI, leaf area index.

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connected by the root system in boreal forests (DesRochersand Lieffers 2001b), hormones that inhibit sucker initiationmay continue to be transported from residual trees to mostof the root system. However, as the number of residual par-ent trees decline, there is likely a decline in the productionof growth inhibitor and the ability to maintain apical domi-nance. Consequently, sucker densities are inversely relatedto basal area retention (Stoeckler and Macon 1956) or to re-sidual canopy cover (Huffman et al. 1999), and removal ofall stems (i.e., clear-cut harvest) consistently promotes thehighest densities of suckers (Zehngraff 1947; Stoeckler andMacon 1956; Schier and Smith 1979; Schier et al. 1985).Partial-canopy retention also appears to limit growth ofsuckers (Zehngraff 1947; Stoeckler and Macon 1956;Farmer 1963; Gifford 1967; Huffman et al. 1999). This ispresumably related to low light conditions limiting photo-synthesis, but growth might also be constrained by the pref-erential allocation of C to the root system in aspen grownunder shade (Landhäusser and Lieffers 2001, 2002). None-theless, the impact of retention trees on suckering andgrowth appears highly variable and has not been well quanti-fied over a range of ecosites and densities of retention trees(David et al. 2001).

In terms of the timing of harvest, winter logging usuallypromotes abundant suckering and best growth comparedwith spring or summer harvest (Stoeckler and Macon 1956;Steneker 1976; Peterson and Peterson 1992). The physiolog-ical condition of roots likely contributes to differences insuckering ability with season (Bates et al. 1993), as low car-bohydrate reserves (Schier and Zasada 1973) or increasedauxin production (Eliasson 1971a) are thought to occur fol-lowing bud flush. These factors are thought to contribute tothe poor suckering generally associated with early summerharvest. For example, cutting of 20-year-old aspen stands af-ter leaf flush resulted in substantially less suckering com-pared with cutting prior to leaf flush (Weber 1990). Summerharvest will also shorten the growing season for suckers andallow the development of leaf area by competitors, both ofwhich may hinder sucker establishment (Bates et al. 1989).S.M. Landhäusser and V.J. Lieffers (unpublished) havefound that root systems of mature northern boreal aspenclones had low carbohydrate reserves throughout the late falland winter season, while the highest root reserves were mea-sured during August when shoot elongation had ceased andleaves were still green. This might explain why some studieshave noted higher suckering after mid- to late-summer har-vest (Bella 1986; Steneker 1976). However, variation inground scarification by machinery, destruction of competingvegetation, soil moisture content, and related compaction atthe time of harvest are also possible confounding factors thatmay explain these differences.

Machine traffic can have serious impacts on aspen suckerproduction. Machine traffic in thawed and wet conditionscan increase soil bulk density and reduce air-filled porespace (Stone and Elliof 1998; Startsev and McNabb 2001),which has been observed to limit root growth of many treespecies (Standish et al. 1988), including aspen (Stone 2001).Reductions in soil aeration are also thought to limit sucker-ing (Bates et al. 1993) and contribute to reduced growth ofsuckers (Greenway 1999). Scuffing, crushing, or fragment-ing of larger roots (Navratil 1991) and fine roots reduces the

ability of the clone to supply water and nutrient to suckers(Shepperd 1993b). In the case of salvage logging after fire,newly developing suckers are vulnerable to traffic; hencemachine activity during the stage of sucker initiation andearly growth will likely damage or kill many suckers (Stone2001).

While machine traffic and compaction may increase soildensity and reduce aeration, in some soils disturbance mayincrease water-holding capacity by increasing microporosity,thereby decreasing water stress in regenerating suckers(Powers and Fiddler 1997; Powers 1999). Machine trafficmay also result in the destruction of competing vegetation,especially shrubs, which in turn may benefit aspen regenera-tion (Steneker 1976; Bella 1986). Furthermore, scarificationby machine traffic can result in soil mixing and soil temper-ature increases, which could stimulate nutrient release andpossibly enhance suckering and sucker growth.

While substantial, the impacts of traffic are often highlylocalized and depend upon site conditions at the time of traf-fic. Skid trails and landings experience the most disturbanceand are noted for poor regeneration and growth (Navratil1991; Darrah 1991; Bates et al. 1993; Shepperd 1993b;Stone 2001; Stone and Elioff 2000) and high rates of suckermortality (Bates et al. 1993). Compaction and reductions insoil aeration occur most commonly when soils are at fieldcapacity or wetter, and most soil modification occurs in thefirst several passes (McNabb et al. 2001). Furthermore, rut-ting damages and (or) displaces roots, which in associationwith poor aeration (Startsev and McNabb 2001) impairssucker establishment and growth (Stone 2001). Shepperd(1993a) noted that skid trails had densities of live roots lessthan one-third of that from untrafficked areas, and he attrib-uted this higher mortality to either compaction-inducedchanges to the soil environment or direct root damage.Poorly drained sites with fine-textured soils are particularlysusceptible to damage and regeneration problems (Bates etal. 1993; Navratil 1991; Shepperd 1993a). However, even ifthe mineral soil of drier sites is more resistant to compaction(Corns and Maynard 1998; McNabb et al. 2001), the roots inthe LFH layer will still be susceptible to mechanical damagefrom traffic. Impacts of traffic, however, will also dependupon the type of equipment and the harvesting techniquesthat are used. Soil compaction can be reduced by using ma-chines with wide low-pressure tires or tracks (Corns andMaynard 1998), or by using lighter equipment and redistrib-uting unmerchantable slash into areas of travel (David et al.2001). In contrast, random skidding, associated with the in-creasing use of feller–bunchers, increases disturbance fromskid trails (Reed and Hyde 1991, cited in Peterson and Pe-terson 1995), which may result in more extensive soil dam-age (McNabb et al. 2001).

The retention of slash on cutblocks has been shown to re-duce suckering in some cases (Steneker 1976; Bella 1986;Schier et al. 1985; Shepperd 1993b, 1996), particularly in ar-eas where it accumulates (e.g., landings) (Schier et al. 1985;Shepperd 1993b). It has been suggested that slash retentionis not considered a significant problem for suckering onfresh to moist sites; however, the decreased temperaturesthat may result from slash retention on cold, wet sites couldlimit regeneration (Steneker 1976). Slash retention reducedinitial sucker density in harvested stands in east-central Sas-

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katchewan, although by year 5 the effect of slash retentionwas less evident (Bella 1986). The findings from the studiesnoted above suggest that slash removal could be used to pro-mote higher initial densities of suckers in some cases, al-though the longer-term consequences of slash removal onthe nutrition of regenerating aspen stands are not known.

Mechanical site preparationSuckering can be stimulated by site preparation

(Zehngraff 1946; Zillgitt 1951; Maini and Horton 1966b;Weingartner 1980; Alban et al. 1994; Shepperd 2001; Fraseret al. 2003). However, the mechanisms controlling increasedsuckering associated with site preparation are not clear. In-creased sucker production has been attributed to temperatureincreases accompanying soil disturbance (Maini and Horton1966b; Hungerford 1988). However, large differences insuckering among mechanically prepared microsites are oftenassociated with only small differences in maximum soil tem-perature (1–2.5°C) (Fraser et al. 2003), suggesting that otherfactors may be involved. Treatments that separate lateralroots from the base of stumps appear to increase suckering(Shepperd 1996, 2001), perhaps because activated buds orsprouts in the stumps are not able to reestablish some degreeof apical dominance over the adjoining roots (Shepperd1996). Furthermore, it is conceivable that wounding or frag-mentation of roots may influence the hormone balance byinterrupting hormone transport and thereby contribute to in-creased suckering. Site preparation could also impact suckerproduction through its alteration of nutrient and moistureavailability or the elimination of competing vegetation(Zehngraff 1946), but these factors have not been well stud-ied.

Site preparation does not stimulate suckering in all cases,and even where suckering is stimulated there may be nega-tive consequences for growth and wood quality. Harsh sitepreparation treatment such as double disking (Ehrentraut andBrantner 1990), mixing (Frey 2001), and disk trenching fol-lowed by drum chopping (Peltzer et al. 2000) can signifi-cantly reduce sucker establishment, likely because roots areeither destroyed or fragmented and thereby isolated from therest of the clone (Zahner and DeByle 1965). Suckers thatoriginate on small segments with few fine roots have limitedcapability for nutrient and water uptake and must preferen-tially allocate carbon to develop a new root system. Frag-mentation of roots into short lengths thus can diminishsucker growth and survival (Zahner and DeByle 1965;Perala 1978) and likely contributes to observations of re-duced height growth associated with site preparation(Weingartner 1980). Forest floor removal treatments, whichhave been shown to stimulate prolific suckering, may alsocontribute to reduced growth and high mortality (Stone andElliof 1998; Kabzems 2000), although it is unclear whetherthis is attributable to root wounding, nutritional limitations,or moisture stress. Weingartner (1980) hypothesized that de-creased growth observed with forest floor removal could berelated to moisture stress in the clone, driven by increasedevaporation after forest floor removal and (or) increased wa-ter demand by higher densities of suckers. There are alsoconcerns that wounding could increase infection and decay,thereby affecting longer-term growth and quality of suckerorigin stands (Basham 1988; J. Pankuch, unpublished data).

Research synthesis

The following section briefly reviews the major conclu-sions from this review and identifies critical gaps in our un-derstanding of aspen root suckering. A series of conceptualfigures (Figs. 1, 2, and 3) are presented to summarize theseideas. We suggest that the variability both within and amongsites in sucker development is a function of (i) root abun-dance and distribution within a stand following disturbance,(ii) the specific physiological and environmental conditionof roots, and (iii) the growing conditions under which thesuckers establish. We acknowledge that this form of concep-tualization does not illustrate interactions between differentfactors, which most certainly exist. However, our goal was toidentify the specific contribution of a factor, recognizing thatmany studies in the past have confounded numerous factors,thereby making interpretation and identification of the criti-cal drivers difficult.

Root distribution and abundanceWe expect that the availability of roots capable of sucker-

ing will affect sucker regeneration dynamics across a sitefollowing disturbance. Densities of viable roots will be afunction of stand condition (basal area, leaf area index, andunderstory development) before disturbance, differencesamong clones in rooting activity (root densities and rootingdepths), and the extent of root loss attributable to effects ofdisturbance (waterlogging and harvesting damage) (Fig. 3).The following are likely the most important site-relatedquestions to be addressed by further research:(1) What is the relationship between sucker density and

predisturbance stand condition (leaf area, basal area,stand health)?

(2) What is the effect of waterlogging after disturbance onsucker establishment?

(3) What is the relationship between sucker distribution anddensity and root distribution and density?

(4) How are root density and subsequent sucker establish-ment affected by the amount of understory shrub, herb,and grass competition prior to and following disturbance?

Sucker initiationThe initiation of suckers from buds developing on the root

surface is governed primarily by the activity of growth regu-lators, which are influenced by the external root environment(Fig. 1). The physiology of sucker initiation remains poorlyunderstood, and further systematic investigation of the rolesof different growth regulators (e.g., using the criteria devel-oped by Jacobs (1959)) is needed. Soil temperature, nutrientavailability, and soil moisture conditions are the likely exter-nal factors that affect sucker initiation to some degree, whilewounding or severing of the root system may further influ-ence sucker initiation. Nonetheless, the following questionsalso remain to be answered:(1) What are the seasonal dynamics of cytokinin production

and transport within the clonal root system, and how docytokinins (or other growth regulators) interact with in-hibitors to affect sucker initiation?

(2) In regenerating stands, at what stage does the reestab-lishment of apical dominance (and the suppression offurther sucker initiation) occur?

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(3) Does wounding or severing of the root system promotesucker initiation?

(4) Does the soil moisture condition at the time of sucker-ing affect sucker initiation?

(5) How do cold soil temperatures (below 12°C) affectsucker initiation?

(6) How do changes in soil chemistry (nutrient availability,pH) following disturbance affect sucker initiation?

Sucker growthSucker growth is influenced by a large number of factors

(Fig. 2). The positive contributions of root carbohydrate re-serves, warm soil temperatures, mesic moisture conditions,and high availability of light and nutrients to vigorous suckergrowth are well understood. Similarly, the negative impacts ofdrought, waterlogging, disease, defoliation, and competitionon sucker growth are reasonably well recognized. Neverthe-less, the following important questions remain:(1) Do high initial densities improve sucker growth and

long-term stand productivity?(2) Does stand condition before disturbance affect sucker

growth, for example, through it effects on the vigour ofthe root system?

(3) How does wounding and severing of the root system af-fect the longer-term growth and quality of the stand?

(4) Do differences in the growth rates of emerging suckersmediate survival and thereby affect initial sucker density?

(5) Do competitors, such as C. canadensis, release allelo-pathic compounds that might diminish growth in aspen?

AcknowledgementsWe thank Erin Fraser, Dave Harrison, Richard Kabzems,

Tim Conlin, and Uldis Silins for discussions of the suckeringproblem, and Canadian Forest Products Ltd. and Forest Re-newal BC for project funding.

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