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Tamm Review: Seedling-based ecology, management, and restoration in aspen (Populus tremuloides)

October 2018
Forest Ecology and Management 432

DOI:10.1016/j.foreco.2018.09.024

Project: Aspen ecology and carbon allocation

Authors:

University of Alberta

Quaking or trembling aspen (Populus tremuloides Michx.) is a foundational tree species, which is native, common, and broadly distributed in North America. The ecology of aspen has been extensively studied throughout its range, but both research and forest management practices have focused primarily on its ability to regenerate asexually via root suckering. The seed-based reproductive ecology of aspen has received comparatively little attention, and information on the underlying processes, mechanisms, and requirements of seed regeneration tends to be scattered, somewhat anecdotal, or based only on localized research efforts. Here we review and explore some of the variables that influence the sexual reproduction and early establishment of aspen. We focus this review on western North America, where trembling aspen plays a dominant ecological role and may be disproportionately impacted by climate change. This synthesis presents existing information and identifies critical knowledge gaps in our understanding of seed-based aspen regeneration, in particular as it relates to flowering and seed production, as well as germination, first year growth, and survival of aspen seedlings. This information is discussed further in the context of aspen ecology and its application in both passive and active management approaches to aspen seedling regeneration and restoration.

Seed dispersal and ripened catkin (inset) of aspen (right panel), seed with pappus (top left panel), and accumulation of seed in depressions and sheltered areas (bottom left panel; photograph by Darren McAvoy).

…

Different stages of early aspen seedling development. A one-day-old germinant with the associated coronet and cotyledons, the two-leaf (top) and four-leaf stage (bottom) of and the different shapes of the first true juvenile leaves. Drawing on the left shows the rapidly developing taproot after about 4-5 days (Drawing by Sandy Long).

…

One-year-old dormant aspen seedlings with high root:shoot mass established from seed in a natural soil. One-year-old aspen seedling established in a cutblock (Alberta, Canada).

…

Passive aspen seedling establishment with shelter from coarse woody debris (top left (photograph by Karen Mock) and right panel) and in a concave microsite position after mechanical site preparation (mounding) for pine regeneration (bottom panel).

…

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Forest Ecology and Management

journal homepage: www.elsevier.com/locate/foreco

Tamm Review: Seedling-based ecology, management, and restoration in

aspen (Populus tremuloides)

Simon M. Landhäusser

a,⁎

, Bradley D. Pinno

, Karen E. Mock

Department of Renewable Resources, University of Alberta, Edmonton, Alberta T6G 2E3, Canada

Wildland Resources Department and Ecology Center, Utah State University, 5230 Old Main Hill, Logan, UT 84322, United States

ARTICLE INFO

Keywords:

Aspen regeneration ecology

Aspen sexual reproduction

Early seedling establishment

Nursery practices

Passive and active aspen restoration

Quaking aspen

Trembling aspen

ABSTRACT

Quaking or trembling aspen (Populus tremuloides Michx.) is a foundational tree species, which is native, common,

and broadly distributed in North America. The ecology of aspen has been extensively studied throughout its

range, but both research and forest management practices have focused primarily on its ability to regenerate

asexually via root suckering. The seed-based reproductive ecology of aspen has received comparatively little

attention, and information on the underlying processes, mechanisms, and requirements of seed regeneration

tends to be scattered, somewhat anecdotal, or based only on localized research eﬀorts.

Here we review and explore some of the variables that inﬂuence the sexual reproduction and early estab-

lishment of aspen. We focus this review on western North America, where trembling aspen plays a dominant

ecological role and may be disproportionately impacted by climate change. This synthesis presents existing

information and identiﬁes critical knowledge gaps in our understanding of seed –based aspen regeneration, in

particular as it relates to ﬂowering and seed production, as well as germination, ﬁrst year growth, and survival of

aspen seedlings. This information is discussed further in the context of aspen ecology and its application in both

passive and active management approaches to aspen seedling regeneration and restoration.

1. Introduction

Quaking or trembling aspen (Populus tremuloides Michx.) is the most

broadly distributed native tree species in North America, with a range

spanning 111° of longitude and 48° of latitude (Little, 1971), occurring

from sea level to 3505 m (Perala, 1990). Aspen is considered an early

successional species that can re-occupy a site quite readily after dis-

turbance through vegetative sucker regeneration from its large under-

ground root system. Aspen has also been considered a ‘foundational

species’ (Ellison et al., 2005), due to its importance in community

structuring and support of a disproportionately high level of plant, in-

sect, and vertebrate diversity (Mills et al., 2000; Rumble et al., 2000;

Simonson et al., 2001; Stohlgren et al., 1997a, 1997b). This is parti-

cularly true in the drier landscapes of western North America and in the

boreal mixedwood forests, where aspen is often the dominant decid-

uous forest tree species. Aspen can be an important source of mer-

chantable wood and ﬁber, especially in the boreal distribution of its

range (David et al., 2001; Peterson and Peterson, 1995), and it provides

other important services throughout its range such as wildlife and li-

vestock forage and shelter, and recreational/aesthetic value (DeByle

and Winokur, 1985; Peterson and Peterson, 1992 and references

therein).

Ecologically, aspen has traits typically associated with ruderal spe-

cies, including the production of large numbers of easily dispersed but

poorly provisioned seeds, rapid establishment following ground dis-

turbance events, a need for easily available resources, and poor com-

petitiveness with other species. Once established, however, aspen

clones are very persistent, and can provide long-term, stable ecosystems

over a wide range of soil, climatic, and disturbance conditions

(Mueggler, 1985). This combination of attributes, along with re-

markably broad ecological amplitude, makes aspen an excellent species

for ecological restoration (including reclamation, reforestation, and

aﬀorestation) following ﬁres, mining, bark beetle outbreaks, timber

harvesting and other disturbances. The need for increased restoration of

aspen is also anticipated due to the eﬀects of changing climates, par-

ticularly in the warmer, drier portions of its range in both Canada and

the U.S. (Rehfeldt et al., 2009; Zoltai et al., 1990). Finally, because

aspen can serve as a fuel break in low- to moderate-intensity ﬁres

(Fechner and Barrows, 1976; Fisher, 1986; Van Wagner, 1977), it can

potentially be a valuable species for strategically establishing barriers

and defensible spaces in ﬁre-prone landscapes. However, the seed-

based reproductive ecology of aspen is incompletely understood and

https://doi.org/10.1016/j.foreco.2018.09.024

Received 27 July 2018; Received in revised form 13 September 2018; Accepted 15 September 2018

⁎

Corresponding author.

E-mail address: Simon.Landhausser@ualberta.ca (S.M. Landhäusser).

Forest Ecology and Management 432 (2019) 231–245

Available online 21 September 2018

(http://creativecommons.org/licenses/BY/4.0/).

poorly synthesized, limiting the eﬀectiveness of aspen establishment

and restoration practices.

This knowledge gap is largely due to the clonal nature of the species.

Aspen is known for its ability to regenerate asexually via root suckering

(Frey et al., 2003; Schier, 1973) and large, long-lived clones are

common (Barnes, 1966; Fetherolf, 1917). The suckering response in

aspen is suppressed by above-ground growth, and suckers are released

when stems are removed (Campbell Jr. and Bartos, 2000; Schier et al.,

1985; Shepperd, 1996; Wan et al., 2006). Vigorous suckering responses

(e.g. > 100,000 stems per ha; Baker, 1925; Bella, 1986; Navratil and

Bella, 1989; Schier and Smith, 1979) following clear felling have led

managers to rely on coppicing as the primary means of stand re-

generation, while research on seed-based regeneration strategies for

aspen has lagged behind that of other forest trees (Long and Mock,

2012). There are clear advantages to vegetative reproduction from the

root system. Under natural disturbance regimes (i.e. ﬁre) the root

system is much more protected than the aboveground parts of the plant

and gives the species the ability to quickly reoccupy and capture the site

after disturbance due to its interconnected root system and reserves

storage within (Zasada et al., 1987). However, coppicing is obviously

restricted to existing aspen stands and clones; a diﬀerent approach is

necessary for areas where aspen has been lost or, in the case of assisted

migration, where it currently does not exist (Aitken et al., 2008; Gray

et al., 2011; Schreiber et al., 2013).

Another serious disadvantage to complete reliance on vegetative

reproduction is its negative impact on genetic diversity, evolutionary

adaptation, and potentially deleterious mutation accumulation (Ally

et al., 2010). While coppicing can dramatically increase the number of

ramets in a stand, it can only maintain or reduce the numbers of genets

(genetically distinct clones which each originated from a single seed)

(Long and Mock, 2012). Genetic diversity should be a major goal of any

long-term conservation or restoration program. While favorable so-

matic mutations within genets may provide some level of genetic di-

versity and adaptive capacity (Otto and Orive, 1995), sexual re-

combination is necessary for the rapid adaptive evolution of multilocus

traits, particularly with the accelerating pace of environmental and

climate change. Because of extensive clonality in aspen, the number of

stems in a landscape can be a misleading indicator of the genetic di-

versity and adaptive potential or persistence in that landscape (Mock

et al., 2008). Further, reliance on vegetative reproduction alone does

not allow gene ﬂow among populations or across landscapes (Eriksson,

1992), which limits the ability of the species to track climate change.

There is marked regional variation in the proportion of naturally

occurring seed-based recruitment in aspen (Kemperman and Barnes,

1976; Navratil and Bella, 1989). In Canada, Alaska, and the Eastern and

Upper Midwestern portions of the U.S., seedling recruitment appears to

be more common than in the southwestern U.S; however, there is in-

creasing evidence of aspen seedling establishment in recent post-burn

areas in the Intermountain West (Kay and Bartos, 2000; Turner et al.

2003; Fairweather et al. 2014; KM personal observation). This regional

diﬀerence in seed-based recruitment rates may be a reason for the

larger clone sizes (i.e. greater age) frequently observed in the south-

western U.S. compared to the much smaller clone sizes elsewhere

(Kemperman and Barnes, 1976). Further, diﬀerences are likely driven

by climates, substrates, herbivory levels, and competing vegetation that

reduce seedling survival (Kemperman and Barnes, 1976). There may

also be regional diﬀerences in seed production rates. In the western

U.S., seed production in aspen is less commonly observed than in other

parts of the species range (pers. observations SL & KM), possibly due to

regional diﬀerences in climate patterns and disturbance regimes (Dale

et al., 2001; Graham et al., 1990), phylogenetic diﬀerences (Callahan

et al., 2013), or rates of triploidy (Mock et al., 2012). Nevertheless, seed

production and seedling recruitment do occur at least episodically in

the southwestern U.S. environments (Fairweather et al., 2014; Kay,

1993; Mock et al., 2008; Romme et al., 1997). In Alaska and western

Canada, upslope range expansion in response to disturbance has been

shown to occur via seedling establishment (Landhäusser et al., 2010;

Zasada et al., 1983) suggesting that seedling-based restoration could be

an important, but underutilized, practice for aspen management.

The importance of seed reproduction in aspen is dramatically ap-

parent in the species’ biogeography. The majority of the species’ current

range since the last glacial maximum represents an expansion into

previously glaciated areas (Callahan et al., 2013; Delorme et al., 1977;

Little, 1971). Such rapid expansion following the glaciation would only

have been possible through wind-based seed dispersal. Wind-dispersed

seed is also likely responsible for the high levels of genetic diversity

within populations and the generally low levels of genetic structuring

among populations in northern distribution of aspen (Callahan et al.,

2013). Once established, aspen clones may persist for millennia (Ally

et al., 2010). Given the increasing incidence and current scale of dis-

turbances in forests (e.g. ﬁre, beetle kill, fragmentation) and the in-

creasing rate of climate change, we anticipate an increasing need for

and reliance on seed-based reclamation, reforestation and aﬀorestation

with aspen (Dale et al., 2001). Thus, the factors inﬂuencing seed pro-

duction and seedling recruitment in aspen are critical aspects in its

regeneration ecology and are crucial in the maintenance or restoration

of aspen on the landscape. Here we synthesize and explore the variables

inﬂuencing sexual reproduction and ﬁrst-year seedling establishment in

aspen in western North America. We have focused our review on western

North America because of the ecological dominance and importance of

aspen in these landscapes; however, there are parallels to other regions

in the northern hemisphere where other closely related species such as

Populus tremula L. and P. grandidentata Michx. dominate. Speciﬁcally,

we synthesize existing information on (1) ﬂowering and seed produc-

tion, (2) germination, and (3) ﬁrst year growth and survival, which we

then discuss in the context of both passive and active aspen restoration

approaches.

1.1. Flowering and seed production

Aspen is generally dioecious, although instances of poly-

gamodioecy, monoecy, and intersexual trees have occasionally been

documented (Pauley and Mennel, 1957; Strothmann and Zasada, 1962;

Wyckoﬀ and Zasada, 2008 and references therein). In most localities,

staminate: pistillate clonal ratios are 1:1, but male-biased ratios have

occasionally been noted (Baker, 1918; Pauley and Mennel, 1957;

Schreiner, 1974), and in one western U.S. study, males were found to

occupy higher elevations and harsher sites than females (Grant and

Mitton, 1979). The generality of these patterns is diﬃcult to assess, as

large proportions of trees and clones may not ﬂower in a given year,

and because clonal boundaries within stands are often cryptic

(Einspahr, 1960; Mock et al., 2008).

Flowering time is driven primarily by air temperature (Fechner and

Barrows, 1976; Moss, 1960), and has been shown to vary by up to

3 weeks from year to year in the same clone (Campbell Jr., 1984; Jones

and Schier, 1985; Perala, 1990). Early spring emergence of ﬂowers can

lead to frost damage and ultimately catkin loss if early spring warming

is followed by a hard frost (Schier et al., 1985). We anticipate that

climate change will exacerbate this phenomenon through diminishing

spring snowpacks, resulting in early warm-up and reduced cold buf-

fering (Inouye, 2008). High rates of catkin damage or loss can also be

associated with fungal disease or insects (pers. observations SL & KM).

The formation of ﬂower buds occurs during the late summer of the

year prior. Catkin emergence and fertilization generally occur in late

March through May before leaves ﬂush (Fechner and Barrows, 1976;

Moss, 1960; Schreiner, 1974). Aspen ﬂowers are small, relatively in-

conspicuous, unisexual, and are arranged in indeterminate pistillate or

staminate catkins (aments) (Fig. 1). This arrangement facilitates the

wind dispersal of both pollen and seeds (Peterson and Peterson, 1992).

The entire ﬂowering process, from catkin appearance to seed matura-

tion, requires 4–6 weeks and is completed in the early spring prior to or

during leaf expansion (McDonough, 1979). Seeds ripen in May or June,

S.M. Landhäusser et al. Forest Ecology and Management 432 (2019) 231–245

232

although timing can vary with weather and geography (Einspahr and

Benson, 1964; Perala, 1990). The densely haired bracts subtending the

ﬂowers make the catkins appear ﬁnely haired when they emerge from

the bud scales and before they expand (Fig. 1). As they begin to expand

and mature, bracts are more separated and the appearance of the cat-

kins becomes dominated by both the stamens and stigmas, which are

reddish in color. As they expand, both male and female catkins become

pendulous and extend to approximately 5–10 cm in length (Perala,

1990). Male catkins become quite ﬂexible as they ripen, and can often

be distinguished from the more rigid female catkins at a distance in the

ﬁeld. The two-chambered ovaries are green, ﬂask-shaped, and 5–7 mm

long, and produce a capsule as a fruit (Fechner and Barrows, 1976).

Individual capsules can contain approximately 6–10 seeds, and catkins

contain approximately 70–100 capsules (Jones and DeByle, 1985b).

The proportion of developing capsules and viable seeds per capsule

vary by genet, within and between trees, and across years. Triploid

genets, which are common in the western U.S. (Mock et al., 2012), have

been observed to produce catkins (either male or female; KM un-

published data), although these are expected to be largely sterile.

Flowering can begin as early as two years after planting, but trees may

not produce heavy seed crops until 10–20 years of age (Maini and

Crayford, 1968; Schreiner, 1974; Stoeckeler, 1960).

Aspen can produce proliﬁc seed crops. Maini and Crayford (1968)

estimated that a single tree can produce over 1.6 million seeds in a

season with about 700,000 to 1 million seeds per kilogram (Maini,

1968; Schreiner, 1974; United States Department of Agriculture, 2018).

Seed production can vary by year and by clone, but generally occurs

between mid-May and mid-June (Fechner and Barrows, 1976;

McDonough, 1985; Moss, 1938; Schreiner, 1965, 1974). Within a clone,

ﬂower production can vary among ramets or branches within a ramet,

depending on ramet age and condition, but patterns have not been well

described over space and time. Stress-induced ﬂowering has been ob-

served and stem girdling has been used to induce ﬂowering (Pauley and

Mennel, 1957). Periodicity of aspen seed production (i.e. masting), at

both the tree and clone level, has been suggested but not well docu-

mented (Maini and Crayford, 1968; McDonough, 1979; Mitton and

Grant, 1996; Santamour, 1956; Schreiner, 1974; Strothmann and

Zasada, 1962).

Seeds are initially a translucent green, and when fully ripened, seeds

attain a light brown color. Individual aspen seeds are small (approxi-

mately 1–2 mm), and when dispersed from catkins they are attached

loosely to a network of long, white, silky hairs (pappus) which expand

from the capsule and can carry the seeds long distances (e.g. several

km) via wind dispersal. In heavy seed production years, accumulation

of pappus containing the seeds can cover the ground locally, settling

into low areas and against windbreaks (Fig. 2).

Fig. 1. Diﬀerent stages of male (left) and female (right) catkin and ﬂower development, detailed male and female ﬂower, closed and opened capsule with protruding

pappus and a seed with the pappus attached (drawings by Sandy Long).

S.M. Landhäusser et al. Forest Ecology and Management 432 (2019) 231–245

233

1.2. Seed germination and initial root development

Aspen seeds have no dormancy and can germinate immediately

after ripening if provided with adequate moisture. Seed viability rates

are typically quite high (> 95%; Maini, 1960; Mitton and Grant, 1996;

Perala, 1995). However, seeds remain viable in the ﬁeld for only a few

weeks even under most favorable natural conditions (low ambient

temperature and high humidity) (Fechner and Myers, 1981; Zasada

et al., 1983).

The germination stage is deﬁned by breaking of the seed coat, and

appearance of hypocotyl and cotyledons, prior to development of the

apical meristem (∼2 days) (Fig. 3). Germination is triggered by

moisture, which is imbibed by the seed within a few hours (Wolken

et al., 2010), and can occur between 0 and 37 °C, with an optimum of

15–30 °C (Faust, 1936; Fechner and Myers, 1981; Jones and Cheliak,

1985). Germination can occur without light or even when seeds are

submerged in or ﬂoating on water (Faust, 1936; Perala, 1990). Thermal

tolerances and interactions with soil moisture and humidity during seed

germination can vary by genotype (Fechner and Myers, 1981;

McDonough, 1979). A brush of root hair (coronet) at the base of the

hypocotyl appears within 24 h (Fig. 3), and is a critical mechanism for

early water absorption and substrate attachment prior to radicle de-

velopment (Day, 1944; Yanchevsky, 1904; Young and Young, 1992),

but are easily damaged by inadequate moisture (Moss, 1938; Perala,

1990). Fechner and Myers (1981) suggested that the greatest suscept-

ibility to moisture stress in aspen germinants occurs subsequent to the

formation of the coronet, and likely during the expansion of the coty-

ledons and hypocotyl. The radicle extends to 20–40 mm within 2 weeks

(Wolken et al., 2010), and is also highly susceptible to drying (Maini,

1960). Green cotyledons (usually 2, occasionally 3; Maini, 1960) also

appear within 24–48 h (Fig. 3). The extreme sensitivity of aspen ger-

minants to even minor soil water deﬁcits (Einspahr and Winton, 1976;

Faust, 1936; Fechner and Myers, 1981; McDonough, 1985, 1979, 1975,

1971; Moss, 1938) creates an important vulnerability for seedling

establishment, particularly in years where precipitation does not coin-

cide with the timing of seed production. Kemperman and Barnes (1976)

suggested that this vulnerability to drought was responsible for in-

frequent seedling establishment and the existence of the large clones in

the semi-arid Intermountain West of the US.

1.3. Early seedling development

Aspen seeds are poorly provisioned with little to no endosperm

(Nagaraj, 1952; Simak, 1980), so apart from water the immediate ac-

cess to light is also critical for continued development. This require-

ment for both consistent moisture shortly after ripening, along with full

to partial sun, severely limits seed establishment success rates in many

cases (DeByle and Winokur, 1985; Maini and Crayford, 1968;

McDonough, 1975; Strain, 1964). These conditions, when they occur,

tend to follow ﬁres or other forms of soil surface disturbances at larger

spatial scales, providing appropriate seed beds and microsite conditions

(Barnes, 1966; Fairweather et al., 2014; Greene et al., 1999; Kay, 1993;

Krasnow and Stephens, 2015; Landhäusser et al., 2010; Quinn and Wu,

2000; Romme et al., 1997; Schott et al., 2014; Turner et al., 2003).

Seedling establishment events are particularly recognizable following

such large-scale disturbances, but these conditions may also occur more

frequently at very small spatial scales, potentially creating a mosaic of

clonal sizes and genetic diversity (Gill et al., 2017; Long and Mock,

2012; Mock et al., 2008). Thus, naturally occurring seedling recruit-

ment, particularly in more arid climates, tends to be highly episodic and

spatially varied, reﬂecting what Jelinski and Cheliak (1992) referred to

as “windows of opportunity” (Romme et al., 2005). We suggest in later

sections that these ‘windows’ can be extended (both spatially and

temporally) by targeted management and restoration practices, and

that these practices will be increasingly important for maintaining

aspen-dominated forests under rapidly changing climate regimes.

The development and maintenance of root resources is a core fea-

ture of aspen ecology, buﬀering against water stress, leaf damage, and

Fig. 2. Seed dispersal and ripened catkin (inset) of aspen (right panel), seed with pappus (top left panel), and accumulation of seed in depressions and sheltered areas

(bottom left panel; photograph by Darren McAvoy).

S.M. Landhäusser et al. Forest Ecology and Management 432 (2019) 231–245

234

defoliation (Barnes, 1966). Root growth is an especially critical com-

ponent of early establishment in aspen (Day, 1944; Martens et al., 2007;

Moss, 1938), and the positive eﬀect of higher root carbohydrate re-

serves and root:shoot mass ratios on establishment success may become

more pronounced when nutrients or soil moisture are limited

(Landhäusser et al., 2012a, 2012b). During the ﬁrst year, aspen

seedlings develop primarily ﬁbrous lateral root systems with few tap-

roots (Jones and DeByle, 1985b; Maini and Crayford, 1968 and refer-

ences therein), but may also produce suckers (Brinkman and Roe,

1975). Root and shoot growth and their ratio are impacted by both

growing conditions and genetic source (Jelinski, 1993; Pregitzer and

Friend, 1996; Romme et al., 2005) (Fig. 4).

Fig. 3. Diﬀerent stages of early aspen seedling development. A one-day-old germinant with the associated coronet and cotyledons, the two-leaf (top) and four-leaf

stage (bottom) of and the diﬀerent shapes of the ﬁrst true juvenile leaves. Drawing on the left shows the rapidly developing taproot after about 4–5 days (Drawing by

Sandy Long).

Fig. 4. One-year-old dormant aspen seedlings with high root:shoot mass established from seed in a natural soil. One-year-old aspen seedling established in a cutblock

(Alberta, Canada).

S.M. Landhäusser et al. Forest Ecology and Management 432 (2019) 231–245

235

Aspen seedlings have an indeterminate growth strategy, and typi-

cally attain a height of between 15 and 60 cm in the ﬁrst growing

season when conditions are not limiting, with lateral roots extending

30–40 cm (Day, 1944; DeByle, 1964; Moss, 1938; Perala, 1990; Strain,

1964). Aspen seedling shoot growth corresponds closely with root

growth and function (Landhäusser et al., 2012b) and ﬁrst year roots are

primarily limited to the upper 20 cm of soil (Pregitzer and Friend,

1996), so competition with other plants for water and nutrients in this

root zone (e.g. grasses) can be a serious constraint on seedling growth

and success (Bockstette et al., 2017; Landhäusser and Lieﬀers, 1998;

Powell and Bork, 2004; St. Clair et al., 2013).

1.4. Water

Continuous, accessible soil moisture is critical for initial establish-

ment of aspen seedlings (Fechner and Myers, 1981; Maini, 1960;

McDonough, 1979), and is thought to be a central driver in the land-

scape-scale distributions of clones and in continental-scale diﬀerences

in clonal sizes (Barnes, 1966; Jones and Cheliak, 1985; Perala, 1990).

At the landscape scale, moisture gradients are expected to be driven by

latitude, elevation, and aspect. In the southern extent of its range,

north-facing slopes or higher elevations will provide the best general

habitats for water retention into the growing season for aspen (Dixon,

1935; Larson, 1944). In northern portions and at higher elevations of its

range, aspen may be more limited by soil temperature than water,

growing best on south and southwest-facing slopes (Perala, 1990).

At the microsite scale, the natural drivers of moisture availability

during the growing season include soil texture, organic matter content,

microtopography (e.g. hillslopes, concavities), and seeps/springs. As

climates change, however, increasing aridity is projected to dramati-

cally decrease the amount of aspen habitat in western North America

(Rehfeldt et al., 2009), and recent large-scale declines of aspen stands in

these landscapes have been associated with drought stress (Anderegg

et al., 2012). Seedlings are particularly susceptible to drought condi-

tions because they lack the resources and resilience of a larger clonal

root mass, although they also suﬀer mortality in standing water

(Howard, 1996; Landhäusser et al., 2003).

1.5. Light

Aside from moisture, the most critical resource for early growth of

aspen seedlings is light (Kaelke et al., 2001), which can be at odds with

the need for continuous access to water. Aspen seedlings are considered

shade-intolerant (Landhäusser and Lieﬀers, 2001; McDonough, 1979;

Moss, 1938). Light restriction due to tree canopy cover (LePage et al.,

2000) limits aspen seedling establishment to stand edges and gaps,

where there may be additional competition for either light (e.g. deep-

rooted shrubs) or soil moisture (e.g. grasses). Compared with other co-

occurring tree species, aspen have more growth and higher rates of

photosynthesis in high to moderately high light levels, but are at risk for

lethal carbohydrate shortages in shaded understory conditions (Kaelke

et al., 2001; Landhäusser and Lieﬀers, 2001).

Given its wide geographic distribution, aspen experiences a wide

range of photoperiods and light qualities such as the amount of ultra-

violet light. Growth rates in aspen are known to be impacted by pho-

toperiod (Vaartaja, 1960), and photoperiod responses have been shown

to have a genetic basis (Ingvarsson et al., 2006), suggesting that local

adaptation to day-length may be an important consideration in seed

transfer zones or assisted migration practices across latitudes. Light

quality showed little eﬀect on aspen growth (Kelly et al., 2015); how-

ever, excessive ultraviolet light can be damaging to leaves, particularly

at high altitudes, and some evidence suggests that the high levels of

tannins in aspen leaves may have at least a partial role as photodamage

inhibitors (Close and McArthur, 2002; Mellway and Constabel, 2009;

Stevens and Lindroth, 2005).

1.6. Soil

Aspen occupies a broad range of soil types across its range, but

achieves the best growth in well-drained, loamy soils high in organic

material (Campbell Jr. and Bartos, 2000; Jones and DeByle, 1985a;

Perala, 1990; Steneker, 1976). For germination and early seedling

growth, soil properties that inﬂuence water retention and availability

are critical (Wolken et al., 2010), but saturated soils prevent gas ex-

change and promote fungal pathogens, and may be problematic in

many sites (Fralish and Loucks, 1967; Kittredge Jr., 1938; Landhäusser

et al., 2003). The availability of bare mineral soils are often cited as a

requirement for successful germination and early seedling growth

(Fralish, 1972; McDonough, 1985), presumably due to the lack of

competition for light and water. However, in environments where

water is limiting, litter, coarse woody debris and moderate shade from

other plants may provide important facilitation for aspen seedlings (de

Chantal and Granström, 2007; Fairweather et al., 2014; Landhäusser

et al., 2010). Surface microtopography or sheltering structures may be

especially important in bare mineral soils remaining after ﬁres, where

black surfaces may further increase risk of high temperatures and

evaporation (Maini, 1968). Aspen seedlings are sensitive to low soil

temperatures, which aﬀect new root growth and soil water uptake

(Landhäusser and Lieﬀers, 1998; Peng and Dang, 2003; Wan et al.,

1999). However, soil temperature can be indirectly aﬀected by other

variables such as shading (Landhäusser and Lieﬀers, 2001), competition

(Bockstette et al., 2017; Landhäusser and Lieﬀers, 1998) and site

characteristics such as ﬂooding (Landhäusser et al., 2003). Little is

known about the nutrient requirements of aspen but aspen seedling

growth and survival has been shown to be responsive to soil nutrient

availability (DesRochers et al., 2003; Hobbie and Chapin III, 1998;

Kinney and Lindroth, 1997; Lu and Sucoﬀ, 2001; Romme et al., 2005;

Van Cleve and Oliver, 1982; Yang, 1991), while overall, aspen is able to

grow over a large amplitude of nutrient conditions (Jones and DeByle,

1985a; Wolken et al., 2010).

1.7. Fungal associations

A broad range of ectomycorrhizal and (less frequently) arbuscular

mycorrhizal fungi are associated with aspen seedlings, which can im-

prove water and nutrient availability (Cripps and Miller Jr., 1993;

Cripps and Miller, 1995; Hankin et al., 2015; Hupperts et al., 2017).

Mycorrhizal fungi have been shown to stimulate growth in aspen in

controlled conditions (Ali, 1985; Cripps, 2000; Landhäusser et al.,

2002), but little is known about the relative importance of particular

mycorrhizal associations in aspen, or how climate, temperature, soil

conditions, stand development stage, or other plants in natural com-

munities may aﬀect these associations (Clark and St. Clair, 2011).

2. Seed-based aspen restoration strategies

The ecological limitations and requirements for successful aspen

seedling establishment, reviewed above, provide an important frame-

work for the design of successful seed-based restoration strategies for

aspen. The importance of particular ecological factors varies with re-

gional climates and likely by genetic sources. The probability of success

and the acceptable costs vs. beneﬁts of seed-based restoration also vary

by site. Thus, appropriate restoration strategies are dependent on spe-

ciﬁc management goals, which in turn are driven by societal values,

landowner and regulatory expectations, and site limitations. There are

two general approaches for seed-based restoration of aspen: passive

restoration, where seedling recruitment occurs passively from naturally

occurring seed rain but can be strategically enhanced by creating ap-

propriate microsites, and active restoration, where aspen seedlings are

nursery grown and then out-planted onto restoration sites. Seeding of

aspen could be considered an intermediate option between active and

passive aspen restoration; however, the information provided in this

S.M. Landhäusser et al. Forest Ecology and Management 432 (2019) 231–245

236

review will show that the collection of seeds and the direct seeding into

prepared sites, would be impractical and high risk because of the high

cost of seed collection, the diﬃculty of dispersing these small seeds, and

the extremely low survival rate of individual seeds when broadcast

across an area.

2.1. Passive restoration of aspen from seed

Past recommendations have presumed that forest managers can do

little to enhance natural aspen seedling establishment (McDonough,

1979), but we suggest that the current prevalence of human activity

throughout many forest lands provides exactly this opportunity. Suc-

cessful passive restoration of aspen from seed does require a naturally

occurring seed rain and exacting climatic conditions for dispersal,

germination, and early establishment, as well as the appropriate mi-

crosites that will provide the necessary resources and conditions for

successful establishment. A range of diﬀerent microsites can be pro-

vided through surface soil disturbances created naturally or artiﬁcially.

For example, natural surface soil disturbances can result from ﬁre,

windthrow, landslides, and ﬂoodplains while artiﬁcial disturbances can

result from forest harvesting and subsequent site preparation, agri-

culture, mining and energy development, and road construction. Nat-

ural seedling establishment has been observed following these events

and our observations can be instructive for the development of proto-

cols that may enhance passive seedling recruitment.

2.1.1. Fire

Aspen seedling establishment following ﬁre has been documented

frequently, although there may be observational bias against other

kinds of seedling establishment events, as seedlings are particularly

easy to visualize against a blackened, otherwise unvegetated substrate

(Long and Mock, 2012). The 1988 Yellowstone ﬁre is a well-known

example of post-ﬁre sexual reproduction with recorded seedling den-

sities ranging from 31 to 46,000/ha (Kay, 1993; Romme et al., 2005).

As expected, diﬀerences in seedling establishment density in this event

depended on both proximity to seed source and site conditions, with

increased seedling density closer to mature aspen seed sources and on

suitable soils lacking intense vegetative competition (Turner et al.,

2003). Other documented examples of aspen seedling regeneration

after ﬁre come from the Alaskan (Zasada et al., 1983) and Canadian

boreal forests (BP, SL personal observations) and the montane forests in

the Intermountain West (Fairweather et al., 2014; Krasnow and

Stephens, 2015) (Fig. 5). Most post-ﬁre seedling regeneration occurs

within a few years following the ﬁre, but can continue for longer per-

iods as long as a seed source and suitable microsites are still available

and have not yet become occupied or shaded by competing vegetation.

Fires do not always result in aspen seedling regeneration, however,

as there can be mismatches in the timing of ﬁre, the quantity and timing

of seed rain, and the climatic conditions. For example, early growing

season ﬁres, which are common in northern boreal aspen forests fol-

lowing dry years (Stocks et al., 2002), may create suitable seedbeds for

aspen establishment in early summer but if dry weather conditions

prohibit aspen seedling establishment, the narrow window of oppor-

tunity may be missed. Later growing season ﬁres, which are relatively

more common in the southern parts of aspen’s range (Westerling et al.,

2003), may create seedbeds for the following year’s seed rain. However,

ﬁre can also create surface conditions that are unsuitable for aspen

seedling establishment due to thick ash layers or increase soil surface

hydrophobicity (Robichaud, 2000).

An eﬀective management strategy when ﬁres in potential aspen

habitat are expected or planned might be to conduct post-ﬁre surveys

for seedling establishment, and plan to protect those areas of higher

stocking with fencing, jackstraw barriers, and/or reduction of ungulate

herbivory pressure if needed. Herbivory from ungulates, livestock, and

insects is a well-known threat to vegetative regeneration in aspen (e.g.

Endress et al. 2012, Seager et al. 2013; Kay and Bartos, 2000 many

more), while much less studied, the impact of herbivory on individual

seedlings with much smaller root systems is expected to be even greater

(e.g. Hansen et al., 2016). Control of ungulate herbivory might include

increased hunting pressure for wild ungulates or temporary reduction

of livestock pressure. For example, successful European aspen (Populus

tremula) seedling regeneration after ﬁre depended on protection from

ungulate browsing which occurred within aggregations of woody debris

(de Chantal and Granström, 2007). Additionally, to avoid reducing

available microsites for establishment and increasing competition, the

operational post-ﬁre seeding of grasses should be avoided for areas

where natural aspen regeneration is expected (Turner et al., 2003),

provided that erosion is not a signiﬁcant threat. In regions where nat-

ural aspen seedling establishment is more common (e.g. Canada and

eastern U.S.) or where herbivore populations are lower, protecting

seedlings is likely to be less important.

2.1.2. Forest harvesting and site preparation

Timber harvesting and site preparation activities can also create

microsites suitable for aspen seedling establishment. Harvesting re-

duces competition for light by removing the canopy, and causes surface

soil disturbance, either through the actual harvest or subsequent site

preparation such as mounding and trenching (Landhäusser, 2009).

These disturbances create suitable microsites, which have micro-

topographical features that can retain soil moisture and are free from

competition by grasses and shrubs, at least temporarily (Fig. 5). Har-

vesting of lodgepole pine in Alberta’s upper foothills followed by site

preparation done to promote pine regeneration was implicated in nat-

ural aspen seedling establishment at densities from 1500 to 10,000

seedlings per ha on sites with appropriate moisture conditions, i.e mesic

and subhygric moisture regimes, (Landhäusser et al., 2010) (Fig. 6).

The probability of natural seedling establishment after harvesting can

likely be enhanced through the use of appropriate harvesting and site

preparation techniques, which create microsites of bare soil to collect

seed and water or snow. The use of heavy equipment does, however,

pose a risk for soil compaction which should be avoided, localized, or

mitigated. In some environments, coarse woody debris can be left to

enhance microsite soil moisture, and/or piled to minimize herbivore

access (Fig. 6). Evidence of seedling establishment from more harvest

studies is lacking, potentially because of intense vegetation competition

after harvesting precludes aspen seedling establishment, or because

seedlings can be missed or misidentiﬁed in sucker-dominated aspen

regeneration (Frey et al., 2003; Long and Mock, 2012). As with post-ﬁre

environments, seeding with competitors (e.g. grasses or other cover

crops) may reduce natural aspen recruitment, and post-harvest mon-

itoring for aspen seedlings could help guide spatially appropriate con-

servation eﬀorts.

Another consideration to enhance natural aspen recruitment after

harvesting would be to leave potential seed trees in cutblocks (Long and

Mock, 2012). During harvesting operations, the aspen component in

stands is often not desirable, particularly for operators targeting con-

ifers. Leaving clusters of mature aspen could help to not only suppress

local suckering (distributing the risk of herbivory losses), but these trees

(if female) may become seed sources for a broad surrounding area. We

recommend that the sex of the trees/clones to be retained in a harvest

operation be determined ahead of time, to the extent possible, and that

mature aspen be left in clusters to retain the beneﬁts of a shared root

system.

2.1.3. Other disturbances

Other disturbances through resource extraction operations such as

mining or road building activities can also create the necessary mi-

crosite conditions for aspen seedling establishment. For example,

naturally occurring aspen seedling densities of up to 20,000–100,000

per ha have been found on phosphate mine dumps in southeastern

Idaho (Williams and Johnston, 1984), on coal mines in Alberta (Schott

et al., 2014) and Pennsylvania (Brenner et al., 1984), and on oil sands

S.M. Landhäusser et al. Forest Ecology and Management 432 (2019) 231–245

237

mines in the boreal forest (Pinno and Errington, 2015). Reclamation

and forest restoration of mined land oﬀers the opportunity to control

even more of the important factors inﬂuencing microsites for aspen

seedling establishment, including topography, soil type and competing

vegetation, than does timber harvesting. Mined land reclamation sites

are often characterized by exposed and reconstructed soil, with low

levels of vegetative competition relative to timber harvest or post-ﬁre

sites. For example, at boreal forest restoration sites, increased aspen

density from natural seedling recruitment was positively associated

with peat-based soils that have high water holding capacity and lower

competition than other reclamation soil types and negatively associated

with fertilization, which resulted in increased competition (Pinno and

Errington, 2015). Surface roughness is also associated with increased

aspen regeneration, likely due to both trapping more seed relative to

ﬂat and compacted microsites and providing a range of microsite types

(Melnik et al., 2018; Pinno and Errington, 2015; Schott et al., 2014).

There is clearly an opportunity to utilize mine reclamation sites across

the species range for aspen restoration.

Although natural aspen seedling regeneration is likely far more

common than previously thought (Long and Mock, 2012), it is still a

relatively rare event, and in many instances after natural or human

disturbances regeneration will not occur either because of a lack of seed

rain, limiting site conditions, or an interaction of the two. The lack of

appropriate microsite conditions for germination may be the primary

limiting factor for natural aspen seedling establishment, particularly in

drier environments including most of the western portion of aspen’s

range, so a more active approach may be required to establish aspen.

This can be accomplished through planting of seedlings, which can

mitigate some of these establishment limitations by growing seedlings

and getting them past the particularly vulnerable period of germination

and early establishment. For this reason, seedling-based restoration

using nursery-grown stock holds great promise for reforestation and

restoration eﬀorts.

2.2. Active restoration using planted seedlings

The production of aspen planting stock can be accomplished using

either vegetative or seedling-based processes. Vegetative propagation of

aspen from root cuttings can be successful (Schier et al., 1985), but the

production of suﬃcient planting material has proven to be a signiﬁcant

limitation (Schier et al., 1985; Snedden et al., 2010), and vegetative

propagation does not increase genetic diversity via sexual recombina-

tion. Therefore, the use of aspen seedlings is currently the preferred

method for producing aspen planting stock (Jacobs et al., 2015;

Macdonald et al., 2015). The collection, processing and storage of seeds

are the initial steps in the production of seedling stock, followed by

nursery production of the seedlings and their outplanting on site. Fol-

lowing the target seedling concept, the most limiting site factors are

Fig. 5. Aspen germinants establishing in a small depression (deer hoof print) two years after a ﬁre in Alberta, Canada (top panel) and aspen germinants in the shelter

of a burned log observed one year following a ﬁre in southern Utah, USA (bottom panel, photograph by Karen Mock).

S.M. Landhäusser et al. Forest Ecology and Management 432 (2019) 231–245

238

used to determine ideal seedling stock types in regards to species- and

site-speciﬁc traits (Puttonen, 1996; Rose et al., 1990). However, while

seedling traits can inﬂuence aﬀorestation success, identifying and po-

tentially mitigating some of the most limiting site conditions, such as

competing vegetation, is also crucial for the success of forest restoration

using seedlings.

Until recently, the knowledge of seedling production techniques for

aspen was based on information available for other commercially im-

portant tree species (mostly conifers in the northern regions)

(Macdonald et al., 2015; Oliet and Jacobs, 2012). However, recent

studies on aspen seedlings and their quality have shown promise in the

ability to manipulate physiological and morphological characteristics

during nursery culture, which has shown to impact early seedling

performance on stressful restoration sites (Landhäusser et al., 2012a,

2012b). Considering that the development of quality seedling stock of

conifers took decades to achieve, the development of quality growing

stock for less commercially important species such as aspen should be

considered to be in its infancy.

2.2.1. Seed collection, processing and storage

Since aspen seeds are wind-dispersed quickly after ripening, the

timing of seed collection needs to be anticipated. The window for col-

lection is generally between three to ﬁve days, but can be extended

during cool and damp weather or shortened to a single day if conditions

are warm, dry, and windy (Smreciu et al., 2013). Female trees should

be monitored regularly (almost daily) during the seed ripening phase,

and it is advisable that female trees (clones) are identiﬁed and pre-

emptively marked prior to leaf ﬂushing, since leaves obscure catkin

visibility. Generally, catkins should be harvested when the enclosed

seeds are a light straw or darker tan color, but this can vary dramati-

cally among clones and collection areas. Another indicator of appro-

priate timing for catkin collection is the presence of capsules showing

the white pappus (Smreciu et al., 2013). Timing of collection is critical

since seeds collected prematurely will not germinate well if at all. Tall

aspen trees might need to be felled to collect catkins, but other means

such as pole pruners, slingshots, and guns (shotgun or small caliber

riﬂes) can be used. Care needs to be taken during collection, as fresh

catkins can heat up quickly from respiration activity when packed too

tightly, resulting in poor seed quality. If capsules are not quite ripe, cut

branches can also be kept for a short period of time (1–2 weeks) in

water (Moench, 1999). Ripe catkins are picked and dried slowly at

room temperature, and seeds can be collected using a steady airstream

to dislodge seeds from the pappus (eg. Smreciu et al., 2013).

Aspen seed can quickly lose viability (within a few weeks) when

stored at room temperature and high humidity, so seeds should be sown

or stored frozen immediately after cleaning. Although aspen seeds have

no natural dormancy, seeds refrigerated at -5°C have been shown to

have 90% viability after 48 weeks (McDonough, 1979; United States

Fig. 6. Passive aspen seedling establishment with shelter from coarse woody debris (top left (photograph by Karen Mock) and right panel) and in a concave microsite

position after mechanical site preparation (mounding) for pine regeneration (bottom panel).

S.M. Landhäusser et al. Forest Ecology and Management 432 (2019) 231–245

239

Department of Agriculture, 2018) and can maintain high levels of via-

bility when stored at -18 to -20 °C for up to 5–8 years (Pinno et al.,

2012; Young and Young, 1992).

2.2.2. Seedling production

Planted aspen seedlings have historically performed very poorly

after out-planting, with high mortality and slow growth (Johnson,

1996; Okafo and Hanover, 1978; Shepperd, 2000; Shepperd and Mata,

2005; Steneker, 1976). Slow initial growth is not always related to

competition (Einspahr and Benson, 1964) or resource limitations (van

den Driessche et al., 2003), suggesting that planting stock quality may

be a factor in poor establishment and growth of seedlings.

Recent work indicates that aspen seedling performance can be re-

lated to morphological and physiological characteristics of the seed-

lings, which can be manipulated during nursery production. This allows

seedlings to be tailored for speciﬁc site conditions (Fig. 7). For example,

on exposed upland forest reclamation sites, where evaporative demands

are high and soil moisture is often limiting, seedlings with high root:-

shoot ratios should have an advantage (Landhäusser et al., 2012a). As

another example, on nutrient-limited sites, nutrient-loaded aspen

seedlings performed much better than seedlings with lower tissue nu-

trient concentrations (Salifu et al., 2009; Schott et al., 2016). By con-

trast, on sites with vegetative competition, there will be trade-oﬀs be-

tween physiological and morphological characteristics (Villar-Salvador

et al., 2012) depending on the type of competition (i.e. above vs. below-

ground competition). For example, on grassy sites with signiﬁcant

above and below-ground competition, tall aspen seedlings experienced

little light competition; however, these tall seedlings performed more

poorly than a much shorter stock type that experienced light competi-

tion, but had higher root:shoot ratios and reserve concentrations

(Landhäusser et al., 2012b; Le, 2017). Seedling characteristics of aspen

will also play a role in their response to herbivory. Characteristics such

as nutrient and carbon reserve status have shown to aﬀect the seedlings

allocation to chemical defense vs. growth, which inﬂuences not only the

damage to or the recovery of an aﬀected seedling but also the ﬁtness of

the herbivore (Osier and Lindroth, 2001; Lindroth and St. Clair, 2013;

Najar et al., 2014; Cole et al., 2016). Just as root:shoot ratios and re-

serve status can be manipulated in the nursery through growing con-

ditions and genotype selection, manipulation of defense chemistry in

aspen seedlings is likely possible in a nursery setting and represents an

exciting area for future research.

2.2.3. Nursery practices

Nursery practices for aspen were originally described for P. tremula

by Barth (1942) and later reﬁned for P. tremuloides (Benson and

Einspahr, 1959; Einspahr, 1959; Wyckoﬀ and Stewart, 1977). Although

bare-root stock production is possible, most information on seedling

quality and performance for aspen involves containerized stock. Gen-

erally aspen seedlings with high root:shoot ratios perform signiﬁcantly

better in the ﬁeld (Landhäusser et al., 2012a; Martens et al., 2007;

Schott et al., 2016), likely because a larger root system supporting a

relatively smaller shoot would have an increased capacity to supply

water and nutrients to the developing shoot after planting. Ad-

ditionally, seedlings with high root:shoot ratios tended to have high

non-structural carbohydrate reserve (NSC) (i.e. sugars and starch)

concentrations (Landhäusser et al., 2012a; 2012b; Martens et al., 2007).

We expect that the importance of high root:shoot ratios in seedlings

would be particularly important when outplanting into sites where

drought stress is anticipated.

Maximizing both root:shoot ratios and carbohydrate reserves could

potentially result in higher stress tolerance (Landhäusser et al., 2012b).

The positive relationship between NSC reserves and seedling survival

and performance is well established (Canham et al., 1999; Myers and

Kitajima, 2007; Ritchie, 1984), and NSC reserves are known to be cri-

tical for seedlings to survive stresses, such as drought, cold tempera-

tures, and physical and disease damage (Canham et al., 1999; Galvez

et al., 2011; Grossnickle, 2005; Lavender, 1984; Matson and Waring,

1984). High root NSC reserves (particularly soluble sugars) also in-

crease the osmotic potential of roots, providing seedlings with an ability

to extract more water from the soil matrix (Galvez et al., 2011). High

reserve status has also been found to increase the exudation of carbon

from roots (Karst et al., 2017) potentially attracting mycorrhizae that

Fig. 7. Range of aspen stock diﬀerences, using a common seed source, solely achieved by manipulating nursery conditions (Landhäusser et al. 2012a).

S.M. Landhäusser et al. Forest Ecology and Management 432 (2019) 231–245

240

could alleviate drought stress (Landhäusser et al., 2002). Since aspen

seedlings invest heavily in root systems (Martens et al., 2007), and

rapid root growth after planting is considered a desirable characteristic

of planted trees (Grossnickle, 2005), suﬃcient NSC reserves could allow

for early root growth after planting (Eliasson, 1968), while stem NSC

reserves are needed to support the ﬂush of new foliage in the spring

(Landhäusser, 2011).

During nursery production, seedling characteristics, including the

root:shoot ratio and NSC reserves, can be manipulated. Aspen has an

indeterminate growth strategy, which allows it to keep growing when

conditions are favorable. However, there is a direct trade-oﬀ between

photosynthate allocation to growth vs. NSC reserves in roots, with

faster growing seedlings allocating less NSC to reserves (Canham et al.,

1999; Chapin III et al., 1990). During periods of stress, aspen will slow

height growth and the production of new leaf area and in extreme cases

will set bud (Galvez et al., 2011; Landhäusser and Lieﬀers, 1998;

Martens et al., 2007), but will continue to photosynthesize. Martens

et al. (2007) suggested that a manipulation of bud set timing could be

used to increase NSC reserves and potentially lead to improvement of

out-planting performance of aspen seedlings. Further studies have

shown that restricting height growth in aspen while maintaining phy-

siological activity in the leaves and roots successfully diverted both

photosynthates and nutrients to storage rather than to growth (Schott

et al., 2016). On a cautionary note, there have been suggestions of in-

creasing root:shoot ratios in aspen seedlings by top pruning the shoot;

however, top pruning results in the reduction of viable buds, formation

of multi-stemmed seedlings, and change the root:shoot ratio without

improving NSC reserves, all of which could result in poor seedling

growth after outplanting.

There are several methods that can be used to successfully reduce or

terminate shoot growth in aspen, including reduced water availability

(Grossnickle, 2012), nutrition (Landhäusser et al., 2012b) and soil

temperature (Landhäusser and Lieﬀers, 1998), shortened day-length,

and use of growth inhibitors (Landhäusser et al., 2012b). Reducing

nutrition and exposing seedlings to controlled drought are considered

risky in a commercial nursery setting, as seedlings are not treated in-

dividually and therefore the risk of mortality or poor seedling quality is

high. Shortening day-length through blackout treatments has been used

for other species (Grossnickle, 2012) and has shown promise for aspen,

but seedling bud set was found to be highly variable and seedlings may

reﬂush (Landhäusser et al., 2012b), negating the objective to increase

storage in seedlings. Shoot growth of aspen can also be inﬂuenced

chemically by applying a shoot growth inhibitor such as Paclobutrazol.

This chemical compound, often used at low concentrations in the hor-

ticultural industry for slowing growth and has been found to be very

eﬀective in the early termination of aspen shoot growth (Landhäusser

et al., 2012b). Shoot height, root:shoot ratio, and reserve concentra-

tions of the aspen seedlings can be controlled by the timing of its ap-

plication (Landhäusser et al., 2012b; Schott et al., 2013). While seed-

lings can be nutrient-loaded when conventionally grown by inducing

“luxury consumption” (Timmer, 1996; Timmer and Munson, 1991), this

fertilization approach has limited potential for aspen given its in-

determinate growth habit, because additional nutrients will induce

additional shoot growth, decreasing root:shoot ratios. However, if

lasting bud set can be induced, nutrient loading of tissues can occur

without additional shoot growth (Schott et al., 2013). Growing aspen

seedlings outside of a greenhouse has also shown some promise in

producing seedling with higher root:shoot ratios and higher NSC con-

centrations (Kelly et al., 2015). Currently the production of aspen

seedling stock occurs under controlled greenhouse conditions opti-

mizing growth. Under outside conditions, seedlings are predisposed to

periods of environmental stress due to the combined increases in light

intensity, wind and temperature (Niinemets et al., 1999). Non-lethal

stress has commonly been found to decrease plant growth more than

photosynthesis limitations (Chaves et al., 2009), potentially leading to a

greater accumulation of NSC and greater carbon allocation to roots

(Coutand et al., 2008; Galvez et al., 2011; Villar-Salvador et al., 1999).

While there is a greater pool of information available for containerized

aspen seedlings, information on the performance and seedling quality

of bare-root aspen seedlings is currently lacking. Bare-root stock can be

generated by direct seeding or by planting one-year old container

seedlings into bare root ﬁelds, where seedlings are grown for one

season. During the fall lift, the seedlings are often heavily root- and

shoot-pruned so they can be economically packaged and stored.

2.2.4. Seedling storage

The timing of planting (see below) will determine the date that a

seedling is lifted and whether overwinter storage is necessary. Time of

lift will aﬀect the characteristics of the seedlings as they are in diﬀerent

physiological and morphological stages. For example, Landhäusser

et al. (2012a) showed that summer-planted (lifted 3rd week of August)

seedlings had lower root volume, root dry mass, root to shoot ratio and

NSC reserves compared to fall-planted (lifted late September) or spring-

planted (lifted in November and stored frozen until spring) after ﬁrst

growing season. If seedlings are to be planted in the spring, seedlings

generally are lifted in the late fall and then bagged and packed in waxed

boxes and stored frozen at a temperature of -3°C. We are not aware of

any study that explores the storage requirements of aspen seedlings;

however, a -3°C storage temperature is known to safely store most

conifer seedlings and does not result in frost damage to their root and

shoots (Stattin et al., 2012; Wang and Zwiazek, 2001). Anecdotal evi-

dence suggests that aspen can potentially tolerate much lower tem-

peratures, but there appears to be an important correlation between

frost tolerance and the NSC reserve status of aspen (Galvez et al., 2013).

2.2.5. Planting and establishment of seedlings

Apart from seedling quality (see above), factors such as handling,

planting procedures, timing of planting, site conditions, and microsite/

planting spot selection inﬂuence the successful establishment and

growth of tree seedlings on outplanting sites (Davis et al., 2010;

Franklin et al., 2012; Grossnickle, 2012; Löf et al., 2012). However,

there is little or no information for most of these factors and their re-

lationship to planting success (Landhäusser et al., 2012a). The timing of

planting can also aﬀect outplanting performance of seedlings. Fall and

winter plantings of aspen are preferred since they use dormant seedling

stock. Spring- and fall- planted seedlings had 44% greater height

growth than summer planted seedlings (Landhäusser et al., 2012a).

A wide range of site preparation techniques has been developed for

reforestation using other species, but very few studies have addressed

this issue with aspen seedlings. Generally, site preparation can be used

to improve resource availability and manipulate abiotic and biotic

conditions such as shade, soil moisture and temperature, and particu-

larly competition that might limit early establishment (Jacobs et al.,

2015). Site conditions can be also altered by amending soils with ma-

terials that can provide a direct source of nutrients and/or water. The

eﬀect of amendments on the early establishment on aspen seedlings has

received little attention with most work related to fertilizer type and

application (Schott et al., 2016; Sloan and Jacobs, 2013). Aspen gen-

erally shows a positive response to fertilization in the ﬁeld (DesRochers

et al., 2003); however, some research indicates that if moisture is

limiting, fertilizer eﬀects are only positive in conjunction with irriga-

tion (van den Driessche et al., 2003). Depending on the soil conditions,

the type and composition of fertilizer can have varied results in aspen

(Pinno et al., 2012). For example, in their study, a balanced N-P-K was

best for height growth, root to leaf mass ratio and bud set, while a P-K

and N fertilizer alone resulted in delayed bud set compared and NPK

which could lead to frost damage (Pinno et al., 2012). Overall though,

fertilizer may favor competing vegetation more than it favors aspen, so

it should be used cautiously.

Vegetation management might be required to provide newly

planted aspen seedlings with low competition conditions. Aspen is very

sensitive to competition, particularly grasses (Bockstette et al., 2017;

S.M. Landhäusser et al. Forest Ecology and Management 432 (2019) 231–245

241

Landhäusser and Lieﬀers, 1998; Schott et al., 2016), which compete

primarily via belowground processes (Bockstette et al., 2017; Le, 2017).

While herbicides can be useful tools in suppressing competing vegeta-

tion, they have limited use in aspen establishment, as herbicides are not

selective enough and aspen may be more sensitive to the herbicides

than the competing vegetation. As with passive aspen restoration

practices, ﬁre may be used to reduce competition prior to planting and

protection from herbivory of the young establishing aspen seedlings

may be necessary in some areas.

3. Conclusions

Seedlings are unlikely to become the dominant form of aspen re-

generation of existing aspen forests across its range, given the proliﬁc

suckering potential of many stands. However, aspen seedlings can play

a signiﬁcant role in changing forests at the stand and landscape scale,

particularly in areas where the species is not currently found. Aspen

seedlings may be particularly valuable in climate change adaptation

and assisted migration projects. Given the exacting seedbed, microsite

and weather conditions that need to coincide for natural aspen seedling

to be successful, the impact of changing future climates on aspen

seedling establishment events is diﬃcult to predict. For example,

weather events may become rarer for successful aspen establishment in

a potentially drier climate, but there may be more frequent seed pro-

duction with increased stress. The use of aspen nursery seedlings in

targeted reforestation is a potentially useful approach, but a great deal

of protocol development is necessary before seedling-based approaches

can become operational. Areas of investigation include optimization of

seedling stock quality, assessment of regional diﬀerences in stock re-

quirements, and determining the most appropriate traits and genetic

sources for successful establishment and growth. Some of these vari-

ables need also to be adapted to anticipated future climates.

For other management applications, the encouragement of aspen

seedling establishment after timber harvest or wildﬁre can be helpful in

the conversion of conifer-dominated forests to more deciduous-domi-

nated forests, reducing the threat of wildﬁre in surrounding commu-

nities. For that, forest management practices and site preparation

techniques can be altered to increase aspen seedling abundance through

microsite creation, strategic retention of mature aspen seed trees, and

the strategic planting of aspen seedlings across the landscape. However,

there is likely more work to be done in order to better predict seed crop

quality and abundance from both internal (e.g. tree age and size) and

external (e.g. weather) factors. Further, it may even be possible to in-

duce ﬂowering through applying stressors and thereby increasing the

potential for seedling establishment following disturbance. The timing

of these inductions would be critical for maximizing success given the

relatively short time frame for establishment success.

Acknowledgements

We thank Jim Long and Caren Jones for their comments and edits

on this manuscript. Sandy Long created the line drawings and unless

acknowledged in the caption of ﬁgures, all photographs are provided by

SML. Work was supported by a discovery grant (2016-04686) to SML

and this collaboration with KEM was supported in part by the Utah

Agricultural Experiment Station, project UTA01291.

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S.M. Landhäusser et al. Forest Ecology and Management 432 (2019) 231–245

245

Terminal velocities and falling patterns correlate with morphology of diaspores in wind-dispersed forestry species

Article

Full-text available

Aug 2022
TREES-STRUCT FUNCT

Key message Wing loading, diaspore type (round-winged vs. single-winged), and aerodynamic motion (autogyro vs. floater) influence the terminal velocity of wind-dispersed diaspores and falling patterns. Abstract The dispersal ability of diaspores dispersed by wind can be reflected in the terminal velocity of the diaspore. Therefore, we measured the terminal velocity of wind-dispersed diaspores in 17 major forest and urban tree species in South Korea and tracked falling diaspore patterns up to the achievement of terminal velocity using the video camera recording method. In addition, the morphological characteristics of the diaspores were measured, and their effect on diaspore terminal velocity tested. Chamaecyparis obtusa (2.66 m s⁻¹) had the highest terminal velocity, whereas Picea abies (0.61 m s⁻¹) had the lowest terminal velocity. Falling diaspores achieved terminal velocity through (1) the oscillating falling pattern of floater diaspores, with a constant descent velocity with minor increases and decreases; (2) the decelerating falling pattern of single-winged diaspores, with accelerating descent velocity followed by rapid deceleration to terminal velocity; or (3) the accelerating falling pattern of round-winged autogyro diaspores, with descent velocity increasing steadily up to terminal velocity. The terminal velocities of single-winged diaspores were significantly lower than those of round-winged diaspores. Although there were cases of similar terminal velocity between species in the same genera (e.g., Abies, Pinus), there were large intraspecific differences in terminal velocity within the same genus due to morphological differences (e.g., Acer). The measured terminal velocities could be applied in simulations for diaspore dispersal distances for forestry tree species. The present study explored the relationship between diaspore morphological characteristics and terminal velocity, and is the first to report the dispersal ability of wind-dispersed seeds of major tree species in East Asia. The findings of the present study can be adopted as key input variables in seed dispersal modeling and facilitate the establishment of natural regeneration plans and conservation of endangered species in the wake of climate change.

Coping with environmental constraints: Geographically divergent adaptive evolution and germination plasticity in the transcontinental Populus tremuloides

Article

Full-text available

Jul 2022

Syntheses clearly show that global warming is affecting ecosystems and biodiversity around the world. New methods and measures are needed to predict the climate resilience of plant species critical to ecosystem stability, to improve ecological management and to support habitat restoration and human well‐being. Widespread keystone species such as aspen are important targets in the study of resilience to future climate conditions because they play a crucial role in maintaining various ecosystem functions and may contain genetic material with untapped adaptive potential. Here, we present a new framework in support of climate‐resilient revegetation based on comprehensively understood patterns of genetic variation in aspen. Elucidating species' genetic makeup and seed germination plasticity is essential to inform tree conservation efforts in the face of climate change. Populus tremuloides Michx. (aspen) occurs across diverse landscapes and reaches from Alaska to central Mexico, thus representing an early‐successional model for ecological genomics. Within drought‐affected regions, aspen shows ploidy changes and/or shifts from sexual to clonal reproduction, and reduced diversity and dieback have already been observed. We genotyped over 1000 individuals, covering aspen's entire range, for approximately 44,000 single‐nucleotide polymorphisms (SNPs) to assess large‐scale and fine‐scale genetic structure, variability in reproductive type (sexual/clonal), polyploidy and genomic regions under selection. We developed and implemented a rapid and reliable analysis pipeline (FastPloidy) to assess the presence of polyploidy. To gain insights into plastic responses, we contrasted seed germination from western US and eastern Canadian natural populations under elevated temperature and water stress. Four major genetic clusters were identified range wide; a preponderance of triploids and clonemates was found within western and southern North American regions, respectively. Genomic regions involving approximately 1000 SNPs under selection were identified with association to temperature and precipitation variation. Under drought stress, western US genotypes exhibited significantly lower germination rates compared with those from eastern North America, a finding that was unrelated to differences in mutation load (ploidy). This study provided new insights into the adaptive evolution of a key indicator tree that provisions crucial ecosystem services across North America, but whose presence is steadily declining within its western distribution. We uncovered untapped adaptive potential across the species' range which can form the basis for climate‐resilient revegetation. Todos los estudios muestran claramente que el calentamiento global afecta a los ecosistemas y a la biodiversidad de todo el planeta. Se necesitan nuevos métodos y medidas para i) predecir la resiliencia climática de las especies vegetales fundamentales para la estabilidad de los ecosistemas, ii) para mejorar la gestión ecológica y iii) para promover la restauración del hábitat y el bienestar humano. Las especies clave de amplia distribución, como el álamo temblón, son esenciales para estudiar la resiliencia a las condiciones climáticas futuras, ya que desempeñan un papel crucial en el mantenimiento de diversas funciones de los ecosistemas además de contener material genético con un potencial de adaptación sin explotar. Aquí presentamos una nueva estrategia para promover la revegetación resiliente al clima, basada en patrones bien estudiados de variación genética del álamo temblón. Les synthèses montrent clairement que le réchauffement climatique affecte les écosystèmes et la biodiversité du monde entier. La mise en place de nouvelles méthodes et de nouvelles mesures est alors nécessaire comme outils de prédiction de la résilience climatique des espèces végétales essentielles à la stabilité des écosystèmes. L'objectif est d'améliorer la gestion écologique ainsi que le bien‐être humain et soutenir la restauration des habitats naturels. Le peuplier faux‐tremble représente une espèce clef à large répartition géographique. C'est une cible importante dans l'étude de la résilience aux futures conditions climatiques car cette espèce est essentielle au maintien de diverses fonctions écosystémiques et elle est porteuse d'un matériel génétique avec un potentiel adaptatif encore inexploité. Nous présentons ici une nouvelle structure de soutien à la revégétalisation résiliente au climat, basé sur des patrons de variation génétique chez le peuplier faux‐tremble. Syntheses clearly show that global warming is affecting ecosystems and biodiversity around the world. New methods and measures are needed to predict the climate resilience of plant species critical to ecosystem stability, to improve ecological management and to support habitat restoration and human well‐being. Widespread keystone species such as aspen are important targets in the study of resilience to future climate conditions because they play a crucial role in maintaining various ecosystem functions and may contain genetic material with untapped adaptive potential. Here, we present a new framework in support of climate‐resilient revegetation based on comprehensively understood patterns of genetic variation in aspen.

Predicting the responses of boreal forests to climate-fire-vegetation interactions in Northeast China

Article

May 2022
ENVIRON MODELL SOFTW

Climate change could alter species composition, with feedback on fire disturbances by modifying fuel types and loads. However, the existing fire predictions were mainly based on climate-fire linkages that might overestimate the probability and size of fire disturbances due to simplifying or omitting vegetation feedback. We applied a model-coupling framework that combines forest succession, climate-fire linkages, and vegetation feedback to predict burned area, aboveground biomass, and species composition of boreal forests in Northeast China under climate change conditions. Results showed that climate change and fire would favor the recruitment of deciduous species, but these species need a long-time to replace the existing coniferous species. Burned area would increase with climate change. Climate change, historical and future fire disturbances affect aboveground biomass by altering tree mortality and regeneration. Further studies should address strategies for altering species composition through forest management practices to adaptation climate change and reduce carbon losses from fire.

Seed Dispersal Models for Natural Regeneration: A Review and Prospects

Article

Full-text available

Apr 2022

Natural regeneration in forest management, which relies on artificial planting, is considered a desirable alternative to reforestation. However, there are large uncertainties regarding the natural regeneration processes, such as seed production, seed dispersal, and seedling establishment. Among these processes, seed dispersal by wind must be modeled accurately to minimize the risks of natural regeneration. This study aimed to (1) review the main mechanisms of seed dispersal models, their characteristics, and their applications and (2) suggest prospects for seed dispersal models to increase the predictability of natural regeneration. With improving computing and observation systems, the modeling technique for seed dispersal by wind has continued to progress steadily from a simple empirical model to the Eulerian-Lagrangian model. Mechanistic modeling approaches with a dispersal kernel have been widely used and have attempted to be directly incorporated into spatial models. Despite the rapid development of various wind-dispersal models, only a few studies have considered their application in natural regeneration. We identified the potential attributes of seed dispersal modeling that cause high uncertainties and poor simulation results in natural regeneration scenarios: topography, pre-processing of wind data, and various inherent complexities in seed dispersal processes. We suggest that seed dispersal models can be further improved by incorporating (1) seed abscission mechanisms by wind, (2) spatiotemporally complex wind environments, (3) collisions with the canopy or ground during seed flight, and (4) secondary dispersal, long-distance dispersal, and seed predation. Interdisciplinary research linking climatology, biophysics, and forestry would help improve the prediction of seed dispersal and its impact on natural regeneration.

Using imagery from unmanned aerial vehicles to investigate variation in snag frequency among forest stands

Article

Mar 2022
FOREST ECOL MANAG

Advances in unmanned aerial vehicle (UAV) technology have opened new opportunities for measuring canopy mortality processes through high-resolution aerial imagery. Unlike traditional plot-based sampling, UAVs can easily survey areas several hectares in size that encompass hundreds of canopy trees. The resulting imagery provides extensive data on the number and locations of dead trees (snags), which can be related to neighbourhood conditions and environmental factors that vary among stands. Here, we used a UAV to measure the relative proportions of live and dead canopy trees in stands varying in soil moisture across a mixed forest landscape. Crowns of live trees and snags were first segmented and classified to species from high-resolution canopy imagery. We then modeled whether crowns of each species were alive or dead as a function of tree height, neighbourhood competition, soil moisture, and the relative abundance of conspecifics. Short lodgepole pine (Pinus contorta var. latifolia) trees were more likely to be dead when surrounded by a tall canopy in sites with greater soil moisture, reflecting effects of competition on this shade-intolerant species. Trembling aspen (Populus tremuloides) was more likely to be alive when surrounded by tall neighbours, perhaps because this clonal species can benefit from facilitation through root connections with neighbouring aspen stems. There was a higher frequency of white spruce (Picea glauca) snags in sites where it had a high relative abundance, suggesting strong effects of intraspecific competition for this species. Soil moisture did not appear to have a direct effect on the snag frequency of any of these species, despite pronounced niche partitioning along an elevation-driven moisture gradient. Our models explained 39% and 33% of the variation in white spruce and lodgepole pine snag frequency , respectively, but did not have much predictive power for trembling aspen or total snag frequency. Our results reflect the important role of competition in determining tree mortality, but also indicate that stochastic or unexplained processes account for considerable variation in snag frequency among stands. As UAV technology becomes more widely used by ecologists, it may enable a better understanding of how biotic and abiotic processes produce local variation in canopy mortality.

Wildfire catalyzes upward range expansion of trembling aspen in southern Rocky Mountain beetle‐killed forests

Article

Dec 2021

Aim Climate warming is expected to drive upward and poleward shifts at the leading edge of tree species ranges. Disturbance has the potential to accelerate these shifts by altering biotic and abiotic conditions, though this potential is likely to vary by disturbance type. In this study, we assessed whether recent wildfires and spruce beetle outbreaks promoted upward range expansion of trembling aspen. Location The San Juan Mountains of southern Colorado, USA (37°34′–37°50′N, 106°49′–107°21′W). Taxon Populus tremuloides. Methods We used aerial imagery to determine the upper elevational limit of adult aspen and conducted seedling surveys at and above this upper limit in burned and unburned areas, which had already incurred high canopy mortality due to spruce bark beetle (Dendroctonus rufipennis) outbreaks. We compared characteristics of burned versus unburned bark beetle-killed sites and assessed microsite conditions related to aspen seedling establishment using generalized linear models and interaction indices. Results Aspen seedling establishment occurred upslope of its previous range within burns, but not in unburned areas, despite severe beetle-driven canopy mortality across all sites before the fire. Aspen seedling establishment was associated more with the light and mineral soil created by fire than the presence of nearby seed sources. Aspen seedlings were associated with nurse objects such as logs and rocks at the highest elevations, where these objects may ameliorate a range of stressors associated with the high elevation range boundary. Main conclusions Not all disturbance types are equal in promoting tree species migrations at the leading edge. Range shifts can be highly localized, and microsites are important for driving local range expansions in transitional environments. The mosaic of future disturbances across the landscape will drive forest compositional shifts, depending on the disturbance types and the species they promote.

A Review of Ungulate Impacts on the Success of Climate-Adapted Forest Management Strategies

Article

Full-text available

Dec 2021

An invasive grass and litter impact tree encroachment into a native grassland

Article

Full-text available

Oct 2021

Questions Woody-plant encroachment and invasive plants are two critical factors that negatively impact grass-dominated ecosystems. While studies have extensively investigated these factors individually, research on how invasive species impact the susceptibility of grasslands to encroachment is less common. Using the aspen parkland, an endangered savannah-type ecosystem, we asked how the presence of a widespread invasive grass in North America, smooth brome (Bromus inermis), impacted the growth and survival of one-year old trembling aspen (Populus tremuloides) seedlings. We also asked if plant litter was a potential mechanism of inhibition (as has been proposed for brome litter) or co-existence (as has been hypothesized for aspen litter) in this system. Location Alberta, Canada. Methods We used a manipulative experimental approach to determine if the survival and subsequent growth of planted aspen seedlings was impacted by the presence of smooth brome and manipulation of litter amount and type. Results We found that the presence of smooth brome reduced aspen survival by 57% compared to un-invaded habitats, likely mediated by reduced soil moisture, while litter manipulation had no effect on survival. For surviving seedlings, local context had complex impacts on growth; the addition of aspen litter to brome-invaded communities increased seedling growth while aspen litter additions to native communities resulted in decreased growth. Conclusion These results suggest that invasion by smooth brome will alter the dynamics of aspen establishment in this system, potentially leading to significant changes to this already endangered landscape. Though smooth brome may serve as a barrier to aspen establishment, accumulation of aspen litter from nearby stands to brome patches could lead to faster growth of seedlings in invaded areas at the edge of existing aspen stands. Our results also suggest more generally that the impact of invasive plants on the establishment of native woody plants can be dependent on litter inputs.

Cytotype and genotype predict mortality and recruitment in Colorado quaking aspen ( Populus tremuloides )

Article

Aug 2021

Species responses to climate change depend on environment, genetics, and interactions among these factors. Intraspecific cytotype (ploidy level) variation is a common type of genetic variation in many species. However, the importance of intraspecific cytotype variation in determining demography across environments is poorly known. We studied the tree species quaking aspen (Populus tremuloides), which occurs in diploid and triploid cytotypes. This widespread species is experiencing contractions in its western range, which could potentially be linked to cytotype‐ dependent drought tolerance. We found that interactions between cytotype and environment drive mortality and recruitment across 503 plots in Colorado. Triploids were more vulnerable to mortality relative to diploids and had reduced recruitment on more drought‐prone and disturbed plots relative to diploids. Furthermore, there was substantial genotype‐dependent variation in demography. Thus, cytotype and genotype variation are associated with decline in this foundation species. Future assessment of demographic responses under climate change will require knowledge of how genetic and environmental mosaics interact to determine species’ ecophysiology and demography.

Genotypic variation rather than ploidy level shapes trait expression in a foundation tree species under drought stress and defoliation

Preprint

Oct 2021

With advancing climate change, tree survival increasingly depends on mechanisms that facilitate coping with multiple environmental stressors. At the population level, genetic diversity is a key determinant of a tree species’ capacity to deal with stress. However, little is known about the relative relevance of the different components of genetic diversity for shaping tree stress responses. We compared how two components of genetic diversity, genotypic variation and ploidy level, shape growth, phytochemical, and physiological traits of Populus tremuloides, under environmental stress. In two field experiments we exposed eight diploid and eight triploid aspen genotypes to individual and interactive drought stress and defoliation treatments. We found that: 1) Genotypic differences were critical for explaining variation of most of functional traits and their responses to stress. 2) Ploidy levels generally played a subordinate role for shaping traits, as they were typically obscured by genotypic differences. 3) As an exception to the second finding, we found that triploid trees expressed higher levels of foliar defenses, photosynthesis, and rubisco activity under well-watered conditions, and displayed greater drought resilience than diploids. This research demonstrates that the simultaneous study of multiple sources of genetic diversity is important for understanding how trees will respond to environmental change.

Root competition, not soil compaction, restricts access to soil resources for aspen on a reclaimed mine soil

Article

Full-text available

Mar 2017

Restricted rooting space in response to soil compaction and below-ground competition with herbaceous plants are two main limiting factors for successful reforestation after surface mining. Fine-textured, nutrient rich soils with adequate soil moisture are particularly susceptible to both of these concerns and while there are recognized ways to manage competition, attempts to alleviate soil compaction through mechanical means have produced varying results. While roots of some herbaceous plants may penetrate compacted soil layers, possibly offering an alternative means to overcome physical restrictions, these potential benefits need to be weighed against negative effects from competition with planted trees. We examined the individual and combined impact of soil decompaction (deep tillage) and management of competing vegetation (herbicide) on soil properties, resource availability and above and below-ground growth of aspen (Populus tremuloides Michx.) seedlings on a reconstructed mine soil affected by severe...

Stress differentially causes roots of tree seedlings to exude carbon

Article

Full-text available

Oct 2016

How carbon (C) flows through plants into soils is poorly understood. Carbon exuded comes from a pool of non-structural carbohydrates (NSC) in roots. Simple models of diffusion across concentration gradients indicate that the more C in roots, the more C should be exuded from roots. However, the mechanisms underlying the accumulation and loss of C from roots may differ depending on the stress experienced by plants. Thus, stress type may influence exudation independent of NSC. We tested this hypothesis by examining the relationship between NSC in fine roots and exudation of organic C in aspen (Populus tremuloides Michx.) seedlings after exposure to shade, cold soils and drought in a controlled environment. Fine root concentrations of NSC varied by treatment. Mass-specific C exudation increased with increasing fine root sugar concentration in all treatments, but stress type affected exudation independently of sugar concentration. Seedlings exposed to cold soils exuded the most C on a per mass basis. Through 13 C labeling, we also found that stressed seedlings allocated relatively more new C to exudates than roots compared with unstressed seedlings. Stress affects exudation of C via mechanisms other than changes in root carbohydrate availability.

Heterozygosity, gender, and the growth-defense trade-off in quaking aspen

Article

Full-text available

Jun 2016
OECOLOGIA

Although plant growth is generally recognized to be influenced by allocation to defense, genetic background (e.g., inbreeding), and gender, rarely have those factors been addressed collectively. In quaking aspen (Populus tremuloides Michx.), phenolic glycosides (PGs) and condensed tannins (CTs) constitute up to 30 % of leaf dry weight. To quantify the allocation cost of this chemical defense, we measured growth, defense chemistry, and individual heterozygosity (H obs at 16 microsatellite loci) for male and female trees in both controlled and natural environments. The controlled environment consisted of 12 juvenile genets grown for 3 years in a common garden, with replication. The natural environment consisted of 51 mature genets in wild populations, from which we sampled multiple ramets (trees) per genet. Concentrations of PGs and CTs were negatively correlated. PGs were uncorrelated with growth, but CT production represented a major cost. Across the range of CT levels found in wild-grown trees, growth rates varied by 2.6-fold, such that a 10 % increase in CT concentration occurred with a 38.5 % decrease in growth. H obs had a marked effect on aspen growth: for wild trees, a 10 % increase in H obs corresponded to a 12.5 % increase in growth. In wild trees, this CT effect was significant only in females, in which reproduction seems to exacerbate the cost of defense, while the H obs effect was significant only in males. Despite the lower growth rate of low-H obs trees, their higher CT levels may improve survival, which could account for the deficit of heterozygotes repeatedly found in natural aspen populations.

Populus tremuloides seedling establishment: An underexplored vector for forest type conversion after multiple disturbances

Article

Nov 2017
FOREST ECOL MANAG

Role of microtopography in the expression of soil propagule banks on reclamation sites

Article

Sep 2017
RESTOR ECOL

The legacy propagule banks of salvaged topsoils are excellent sources of plant propagules for reclamation of mine sites; however, earlier studies show that less than 50% of the species found in original propagule banks actually establish. We hypothesize that the expression of this legacy propagule bank is limited by a lack of diversity of microsites and appropriate growing conditions. In an operational-scale field experiment we manipulated topographical characteristics and substrate materials and explored early vegetation establishment on an east- and south-facing slope. Three different site treatments with different microtopographic characteristics: (1) leveled surface, (2) parallel ridges, and (3) large loose piles were created using salvaged upland and lowland forest floor soil materials. Placing materials in loose hills and providing heterogeneity in substrates more than doubled plant abundance, species richness, and increased the proportion of species that require higher soil moisture. Lower micro-elevations and northern microaspects of the microtopographic treatments had up to three times higher soil water content and double the species richness. However, the overall slope aspect had a modulating effect on microtopographic positions. The greatest treatment effect of micro-elevation and microaspect on species richness and plant abundance occurred on the east-facing slope, while the greatest effect of treatment on the proportion of species requiring higher soil moisture conditions was observed on the south-facing slope. Variability in microtopography and substrate can create favorable growing conditions at an operational scale and help express a wider range of species from the legacy propagule bank.

Vegetation associations, Aspen: Ecology and management in the western United States, General Technical Report RM-119

Article

Jan 1985

N.V. De Byle

Host phenology and potential saprotrophism of ectomycorrhizal fungi in the boreal forest

Article

Jun 2016

1. Phenology-induced changes in carbon assimilation by trees may affect carbon stored in fine roots and as a consequence, alter carbon allocated to ectomycorrhizal fungi. Two competing models exist to explain carbon mobilization by ectomycorrhizal fungi. Under the ‘saprotrophy model’, decreased allocation of carbon may induce saprotrophic behaviour in ectomycorrhizal fungi, resulting in the decomposition of organic matter to mobilize carbon. Alternatively, under the ‘nutrient acquisition model’, decomposition may instead be driven by the acquisition of nutrients locked within soil organic matter compounds, with carbon mobilization a secondary process. 2. We tested whether phenology-induced shifts in carbon reserves of fine roots of aspen (Populus tremuloides) affect potential activity of four carbon-compound degrading enzymes, b-glucuronidase, b-glucosidase, N-acetylglucosaminidase and laccase, by ectomycorrhizal fungi. Ectomycorrhizal roots from mature aspen were collected across eight stands in north-eastern Alberta, Canada, and analysed during tree dormancy, leaf flush, full leaf expansion and leaf abscission. We predicted potential extracellular enzyme activity to be highest when root carbon reserves were lowest, should host phenology induce saprotrophism. Further, we anticipated enzyme activity to be mediated by invertase, a plant-derived enzyme which makes carbon available to fungal symbionts in the plant–fungus interface. 3. Root carbon reserves were positively correlated with invertase, suggesting phenology may affect carbon allocation to ectomycorrhizal fungi. However, of the four enzymes, host phenology had the largest effect on b-glucuronidase, but activity of this enzyme was not correlated with root carbon reserves or invertase. Low-biomass ectomycorrhizas had greater potential laccase activity than high-biomass ectomycorrhizas, highlighting discrete functional traits in fungi for litter decomposition. 4. Our results suggest that the decomposition of organic matter may be driven by foraging by fungi for nutrients locked within organic compounds rather than for mobilizing carbon. Furthermore, the potential ability to degrade lignin was more common in low-biomass ectomycorrhizas when compared to high-biomass ectomycorrhizas.

Survival and Growth of Planted Black Spruce, Alder, Aspen and Willow After Fire on Black Spruce/Feather Moss Sites in Interior Alaska

Article

Apr 1987
FOREST CHRON

Seedlings of black spruce, aspen, green alder, and grayleaf willow planted on black spruce/feather moss sites in the boreal forest in interior Alaska survived and grew relatively well over a 6-year period after prescribed burning. Survival of black spruce was significantly greater than that of the broad-leaved species, but height growth was significantly less. Development of feltleaf willow and balsam poplar from unrooted cuttings was poor. Severity of burn appeared to have an important effect on height growth of all species but not on seedling survival. Key words: Planting, Picea, Alnus, Populus, Salix, microsite.

Plant Physiology and Nursery Environment: Interactions Affecting Seedling Growth

Chapter

Jan 1984

D. P. Lavender

Environmental factors (such as light, moisture, nutrients, density, and temperature) and plant physiological factors (such as carbohydrate reserves, hormone levels, frost hardiness, and dormancy) interact to shape growth and survival of coniferous seedlings in nursery fields and after outplanting. Nursery managers can manipulate moisture, nutrients, and density to achieve desired seedling morphology and vigor. However, the annual growth cycle of perennial plants has evolved in response to environmental pressures. When the environment is modified, as with heavy irrigation in a nursery, to permit growth at a time when natural seedlings are dormant, the ensuing phases of the growth cycle will not be properly synchronized with their environments. Seedlings so cultivated lack vigor after outplanting. Nursery managers should aim at keying their cultivation schedules to both environmental conditions and endogenous seedling physiology toensure production of high-quality seedlings.

Shifting ecological filters mediate postfire expansion of seedling aspen (Populus tremuloides) in Yellowstone

Article

Feb 2016
FOREST ECOL MANAG

Determining how ecological filters (e.g., climate, soils, biotic interactions) influence where species succeed in heterogeneous landscapes is challenging for long-lived species (e.g., trees), because filters can vary over space and change slowly through time. Stand-replacing wildfires create opportunities for establishment of tree-species cohorts and can catalyze rapid shifts in where species occur, facilitating unique opportunities for long-term study. We quantified effects of multiple ecological filters on a colonizing cohort of aspen (Populus tremuloides) that established from seed throughout burned lodgepole pine (Pinus contorta var. latifolia) forests after the 1988 fires in Yellowstone National Park (Wyoming, USA) to ask: (1) How have aspen presence, density, and size varied across the postfire landscape, and what filters explain these spatial and temporal patterns? (2) How does aspen above-and belowground biomass vary with postfire lodgepole-pine density? Aspen persisted to postfire year 25 in 58% of the plots in which aspen were present in postfire year 11 (n = 45), and mean stem density declined from 522 to 310 stems ha−1. Mean aspen height doubled (from 29 to 59 cm) over this period. Ecological filters related to climate, competition, herbivory, and soils all differentially affected aspen presence, persistence, and size. Growing season temperature, inter-specific competition, and herbivory also changed through time, altering their effects on the colonizing cohort, and shifting where on the landscape aspen persistence and growth were ultimately favored. Eleven years postfire, aspen were favored at warmer, low elevations; ungulate browsing strongly constrained aspen heights; and competition was unimportant. By 25-years postfire, temperatures warmed nearly 1 °C, and aspen were more likely to persist at cooler, high elevations. Browsing pressure declined, as ungulate populations decreased during this time, but aspen height and basal diameters were constrained by dense, rapidly growing postfire conifers. Landscape mosaics of ecological filters shift over space and time and can facilitate or constrain the persistence and growth of colonizing species. Long-term study of post-disturbance colonizing cohorts uniquely reveal how species are responding to real-time environmental change in heterogeneous landscapes, which will help us better anticipate 21st century species distributions and abundances.

Tamm Review: Seedling-based ecology, management, and restoration in aspen (Populus tremuloides)

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