Producing wild leek in forest farming under northern climates

Lapointe, L., Dion, P.-P., Denis, M.-P., Boulanger-Pelletier, J., Bussières, J. & Bernatchez, A. Department of Biology and Centre for Forest Research, Laval University, Quebec City, Canada. G1V 0A6. Line.Lapointe@bio.ulaval.ca

(Presented at The Future of Ginseng and Forest Botanicals Symposium, July 12-14, 2017, Morgantown, WV)

Abstract

This paper presents the results of experiments we have been running over the past ten years in order to improve wild leek growth under forest farming. Wild leek thrives under low temperatures typical of early spring. Under more northern climates, the plant annual cycle is compressed in time, which reduces bulb growth. Planting wild leek under trees leafing out late (oak, ash or walnut) prolongs wild leek’s growing period and improves annual growth. However, seedlings behave differently from mature plants and can continue their growth under shade conditions in the summertime. High natural plant density negatively affects plant growth and appears to expose the plant to pest outbreaks such as spotted snake millipedes. Partial bulb harvest can improve growth of the remaining bulbs by reducing plant density. Leaf harvest can be sustainable if harvest occurs late in the season and the plant is allowed to recover its initial size before being subjected to another leaf harvest. Organic fertilizers improved plant growth whereas gypsum is recommended when planting in soils low in calcium. The presence of litter, although maintaining the soil slightly cooler than in absence of litter, did not influence plant growth, but improved wild leek survival the year following planting. Soil tilling did not improve survival nor plant growth, but could nevertheless be useful in some sites, in addition to facilitate bulb planting. Further testing is needed to optimize fertilization (formula, application rates and frequency), soil tilling and litter, along with pest management studies.

Keywords:  agroforestry, Allium tricoccum, light response, mineral fertilization, plant density, plant harvest

Introduction

Wild leek or ramp (Allium tricoccum L.) is a well-known forest herb in northeastern USA and eastern Canada, due to its culinary properties. There are even some ramp festivals in spring each year. Wild leek mostly thrives in rich hardwood forests: it is present from Tennessee and North Carolina to the southern part of eastern Canada; and from the East Coast up to South and North Dakota (Flora of North America).

As most forest herbs, wild leek exhibits slow growth rate, yet plant populations can be very dense due to clonal propagation (Nault and Gagnon 1993). Nevertheless, there is great concern regarding the capacity of wild leek to tolerate repeated harvests, especially large-scale harvests to support a commercial market (Nantel et al. 1996; Rock et al. 2004). The species is listed as special concern in Maine, Rhode Island and Tennessee, and as endangered in the province of Quebec, where large-scale harvests occurred in the 1970s leading to the extinction or near extinction of many populations (Couillard 1995). In response to this dramatic decline, the provincial government passed a law that strictly forbids selling of wild leek in Quebec, and stipulates that forest owners can only harvest 50 plants per year for their own consumption. Besides commercial harvests, long-term overabundance of white-tailed deer as well as destruction of habitat due to urbanization both threaten populations. Deer consume wild leek to some extent, although it is not one of its preferred plant species (Anderson 1994).

As for other exploited forest herbs, cultivation under forest farming can be an avenue to pursue in an attempt to reduce the pressure on natural populations while fulfilling the demand from consumers. We thus initiated a series of experiments to characterize the conditions that favour the establishment and yield of wild leek planting under forest farming and to quantify the impact of leaf and bulb harvest on plot yields during the following years. The effects of 1) the light environment in the understory, 2) temperature, 3) litter, 4) soil tillage, 5) fertilizers and gypsum, and 6) plant density on plant growth were quantified in plots established from bulbs. We also measured the impact of different intensities of either leaf or bulb harvest on subsequent plant growth. These studies have furthered our knowledge of the biology of the species, which in turn helped us identify the optimal yield conditions.

Material and Methods

Readers are encouraged to refer to the published papers for the details regarding Material and Methods. The effect of the tree canopy has been published by Dion et al. (2017); the effect of light quantity has been published by Dion et al. (2016a); the fertilization trials have been published by Bernatchez et al. (2013); the effect of plant density and of leaf and bulb harvest has been published by Dion et al. (2016b), and the effect of growth temperature has been published by Bernatchez and Lapointe (2012). Hereafter we described the methods for the latest studies not yet published.

Soil Tillage

Plots (1.65 x 0.9 m) were first established in spring 2014 in two sugar maple forests located in the Argenteuil regional county municipality, in the Laurentides region (45° 39’ N; 74° 20’ W). Two treatments, one tilled and a control not tilled were repeated 5 times on each site, for a total of 20 plots. Litter was first removed and soil tilling was performed using a Pulaski to a depth of 15 cm. Organic fertilizers (55–110–82 kg ha-1 of N–P2O5–K2O) and gypsum (3000 kg ha-1) were then spread over the plot in June 2014 and May 2015, before litter was put back onto the plots (Bernatchez et al. 2013; see Amendments in the Results and Discussion section). Fifty bulbs were planted in each plot in July 2014 at a depth of 5 cm. The following spring, high mortality rates were observed. We moved the few remaining bulbs outside the plots, and planted 50 new bulbs per plot in May 2015. For both plantings, bulbs came from seizure by governmental authorities. Bulbs with a diameter of 10 to 15 mm were selected for the two experiments (Soil Tillage and Litter).

Survival was estimated the following spring based on the number of plants that emerged/number of bulbs planted per plot. Total leaf width was measured at complete leaf unfolding. Bulb diameter was measured in late June after complete leaf senescence. The top of the bulbs were gently dug then the diameter was measured using calipers. For bulbs that divided, we measured each bulb individually, then calculated the diameter of a bulb that would represent the same total surface area as the sum of the individual bulbs (see Dion et al. 2016b for details).

Litter

Plots of the same size as for the Soil Tillage experiment were established in the same two locations. Litter was first removed and soil was tilled before planting. The same doses of fertilizers and gypsum as for the Soil Tillage experiment were incorporated into the plots before planting. Three treatments were compared: no litter, natural litter put back on the plots following tillage, and 3 cm of ramial chipped wood (RCW) spread onto the plots following tillage. The RCW was made of sugar maple branches finely chipped. Each treatment was repeated 5 times for a total of 30 plots. Similarly to the Soil Tillage experiment, a first planting took place in July 2014, and a second planting in spring 2015 with 50 bulbs per plot. Natural litter was removed from the no litter and the RCW plots before the second planting as well as the following spring. Data loggers (iButton, Maxim Integrated, San Jose, CA) were placed at a depth of 5 cm to record soil temperature throughout the year every 2.5h. Mean per day was calculated then averaged over each month. Data presented are for the month of May based on the data recorded in each plot the year planting occurred and the following year. The same plant variables (survival, total leaf width and bulb diameter) as for the Soil Tillage experiment were also monitored.

Results and Discussion

Light environment in the understory

Wild leek senesced later under late canopy closure than under canopies that closed earlier in the season; this longer leaf lifetime translated into larger bulbs over the years (Dion et al. 2017). The composition of the tree canopy thus influences wild leek growth. Tree species that bud burst later, such as Fraxinus, Juglans, Quercus, Tilia or Carya spp, provide a light environment that can favour wild leek growth, at least at the northern limit of its distribution, as the duration of the high light conditions between complete snow melt and aboveground canopy closure decreases from north to south in hardwood forests (Routhier and Lapointe 2002).

Although mature wild leek plants are exposed to high light conditions in spring, this is not the case for seedlings, which grow under the canopy of mature wild leeks especially in dense patches. We noticed that seedlings and juveniles senesce somewhat later than mature plants. We thus wanted to quantify the response of mature plants to light availability in spring compared to that of seedlings and juveniles. All plants were exposed to 60% of incident light for 30 days simulating conditions in the understory in early spring. They then received either 60, 10 or 4% of ambient light until complete leaf senescence (Dion et al. 2016a). Mature plants and three-year-old juveniles senesced much earlier than two-year-old and seedlings even when subjected to the same light conditions. Within each plant size, wild leeks produced larger bulbs under higher than under lower light conditions. However, while mature plants and three-year-old juveniles kept their leaves longer under higher light conditions in order to produce larger bulbs, seedlings senesced earlier under higher light conditions. Timing of leaf senescence of two-year-old juveniles was not affected by light availability. We concluded that seedlings and two-year-old juveniles behave as summer green plants that maintain their leaves for much longer than mature plants which behave as spring ephemerals (Neufeld and Young 2014). Young wild leeks acclimated their leaves to lower light conditions whereas mature plants exhibited no acclimation and induced leaf senescence once exposed to decreased light availability. Seedlings, which appear source-limited, may require a longer time than mature plants to accumulate the carbon reserves necessary to survive until the next year. Mature plants with their much larger leaf-to-bulb ratio can fill their bulb much faster than seedlings, which may have led to the evolution of the spring ephemeral growth habit.

Temperature

Spring ephemerals need to be able to grow at low temperatures since they sprout early in spring. Yet, most plants adapted to grow at low temperatures still perform better at higher temperatures, more typical of summer time (Lapointe and Lerat 2006). We have already shown that other spring geophytes such as trout lily (Erythronium americanum) and spring crocus (Crocus vernus) do grow better at 12/8 °C (day/night temperatures) than at 18/14 °C (Lapointe and Lerat 2006; Badri et al. 2007). Trout lily does even better at 8/6 °C than at 12/8 °C (Gandin et al. 2011). We tested the impact of these three growth temperatures on wild leek growth under controlled growth conditions (Bernatchez and Lapointe 2012). Similarly to the other spring geophytes, wild leek final bulb size was greater at 12/8 °C than at 18/14 °C, but bulb size was smaller at 8/6 °C than at 12/8 °C. This study confirmed that spring geophytes are well adapted to grow at low temperatures to the extent that their growth decreases at higher temperatures. We have previously shown that soil more than air temperatures affect growth of geophytes (Badri et al. 2007).

Litter

When wild leek was grown under different tree species, we noticed a positive relationship between litter thickness in spring time and wild leek survival rate (Dion et al. 2017). Soil temperature under a thicker litter was cooler and less variable than under a thinner litter. As tree litter differs in other aspects than litter thickness, we ran a specific experiment to compare the effect of natural litter, a RCW mulch, and no litter on wild leek survival and growth. We included a treatment with RCW mulch as a potential solution on forested sites or tree plantations where natural litter is degraded by early summer, due to the activity of earthworms (Corio et al. 2009). Plants in this experiment were strongly affected by the bulb mite (Rhizoglyphus robini) which most likely influenced the conclusions we can draw from this study. We reported an increased survival in plots covered with RCW mulch than in plots with no litter (Fig. 1). Natural litter presented intermediate results. The litter treatment did not affect the total leaf area (data not shown) nor the bulb size (Fig. 1). Soil temperature in spring was lower in plots covered with litter or mulch than in plots without litter (Fig. 2). We could expect that soil temperature differences lead to differential growth of wild leek over time. Furthermore, litter — either natural or as a mulch — could lessen evaporation and maintain a higher soil water content, a condition that favours wild leek growth (Nault and Gagnon 1993; Bernatchez et al. 2013).


Fig. 1: Effect of the presence and type of litter on wild leek survival and bulb size. Survival was recorded in early spring and bulb diameter was measured in early summer, the year following planting. RCW: ramial chipped wood. Different capital letters indicate differences among litter treatments, both sites confounded

Fig. 2: Effect of the presence and type of litter on mean soil temperature during the month of May. Soil temperature was measured at the same depth as the bulbs, i.e. 5 cm during the year planting occurred and the following year. RCW: ramial chipped wood. Different capital letters indicate differences among litter treatments, both sites confounded

We found very few impacts of litter or mulch on plant mineral nutrition, as estimated from leaf nutrient content (data not shown). Surprisingly, wild leek absorbed more calcium (Ca) in plots without litter (5.6 ± 0.3 mg g-1) than in plots covered with RCW mulch (4.6 ± 0.2 mg g-1), despite the fact that soil Ca availability is strongly correlated with the rate of Ca mineralization from organic matter (Dijkstra 2003). The absence of a litter might increase the rate at which Ca is released from gypsum through higher temperatures and more rapid rainfall penetration in the soil, explaining the higher absorption of Ca by wild leek. Natural litter degraded faster than RCW mulch (pers. obs.) which could explain the slightly higher concentration of Ca in wild leek under natural litter (4.8 ± 0.2 mg g-1) than under mulch.

Soil Tillage

Tillage is prescribed for most herbs grown under forest farming (Persons and Davis 2005), but takes time and effort. We wanted to compare growth of wild leek following direct planting with that of bulbs planted in tilled soil. In the absence of soil tillage, litter still needs to be removed to spread fertilizers and plant the bulbs before putting the litter back onto the ground. We did not see any impact of soil tilling on either plant survival, total leaf area or bulb size (Fig. 3). Soil tillage did not impact plant mineral nutrition the following year (data not shown). Short-term tillage does not always improve nutrient mineralization as demonstrated in other systems (Kingery et al. 1996; Kristenen et al. 2003). Tillage does not seem necessary, although it certainly facilitates bulb planting. However, as results varied between sites (Fig. 3), we need to test the impact of soil tilling in different types of soils to determine whether tilling would benefit wild leek under specific conditions.

Fig. 3: Effect of soil tillage on wild leek bulb size. Bulb diameter was measured in early summer, the year following planting

Amendments

Wild leek thrives on rich soils with high Ca availability (Rousseau 1974). We thus tested the impact of organic fertilizer and gypsum on its subsequent growth over two years (Bernatchez et al. 2013). Organic fertilizer composition was chosen based on recommendations for cultivated garlic and leek in organic soil and from Nadeau and Olivier (2003) for forest farming of ginseng. We chose Bio-Garden (4–3–6; McInnes Natural Fertilizers, Stanstead, QC, Canada), a granulated slow-release fertilizer made from feather meal, fossil bone meal (natural rock phosphate) and Sul-Po-Mag to which we added more fossil bone meal (0–13–0) to enhance P availability. Two levels of fertilization were tested: 27.5–55–41.3 kg ha-1 (N–P2O5–K2O) and 55–110–82.5 kg ha-1. We combined these fertilizer treatments with the addition of gypsum (Uncalcined Gypsum Products, CaSO4, Georgia-Pacific Gypsum Corporation, Atlanta, GA, USA) at a rate of 3000 kg h-1.

Gypsum had limited impact on wild leek (Bernatchez et al. 2013). We reported higher concentration of Ca in the leaves, but no impact on plant growth over two years. The Ca/Mg ratio was affected by the addition of gypsum. The sites were rich in Ca (2486 to 9344 kg ha-1). We ran a second experiment on these same sites where we modulated the amount of Ca (1000 vs 3000 kg ha-1 of gypsum) and magnesium (Mg) (addition of chelated Mg to attain 75 kg ha-1 vs 41 kg ha-1) to try to establish a better balance between Ca and Mg. Wild leek juveniles exhibited slower growth in plots fertilized with a surplus of Mg compared to plants in control plots (55–110–82.5 kg ha-1 of N–P2O5–K2O; 3000 kg ha-1 of gypsum), whereas reducing the amount of gypsum did not affect plant growth. The addition of gypsum would need to be adjusted as a function of natural Ca availability in the soil as it can greatly improve wild leek growth in soils low in Ca (Ritchey and Schumann 2005).

Mineral fertilization did improve plant growth (leaf width in year 1/leaf width in year 0) the following year compared to unfertilized plants (Bernatchez et al. 2013). They also produced a larger bulb for a similar leaf size. However, these results were only observed the year following the fertilization. Two years after fertilization, size of fertilized plants no longer differed from that of control plants. Nitrogen (N) was the only nutrient that increased in fertilized compared to unfertilized plants and soil analyses indicate no differences among plots two years later. We thus concluded that either fertilizers would need to be applied each autumn (at the time new roots appear), or that fertilization was mainly useful to recover from transplantation shock. Nitrogen appears to be the most limiting macronutrient, based on the N: P ratios recorded. A second experiment was thus conducted in which fertilizers with either more N (110 vs 55 kg ha-1) or less phosphorus (P) (41 vs 110 kg ha-1) were compared to the initial treatment (55–110–82.5 kg ha-1 of N–P2O5–K2O; unpubl. data). We recorded no difference among the three fertilizer treatments in terms of leaf or bulb width. This study indicated that the addition of bone meal (0–13–0) to the Bio-Garden fertilizer is not necessary to insure good growth rate of wild leek.

Plant Density

Wild leek tends to grow in dense patches due to the propagation method by division of the bulb (Nault and Gagnon 1993). Competition among shoots could eventually decrease their growth rate. We tested different planting densities, including densities similar to those recorded in nearby natural populations to quantify the impact of the plant density on plant growth and to determine optimal planting densities (Dion et al. 2016b). Four different densities were tested: 44, 89, 178 and 356 bulbs m-2. Four years after planting, individual plants in the densest plots were smaller than in the three other plot densities. Plant division was also affected by plant density, to the extent that four years after planting we recorded the same number of shoots per plot in the two highest densities whereas in the lowest density there were 50% more bulbs than initially planted. At year 5, mortality started to spread in the plots, starting with the dense plots but eventually affecting all plots in year 6, since they were fairly close to each other. Dying of compact clumps has been reported previously (Nault and Gagnon 1993). The soil was infested with spotted snake millipedes (Blaniulus guttulatus). However, further studies are needed to determine if the millipede can be the initial cause of bulb decay or if another pest or pathogen weakens the plant prior to the attack by the millipede. Considering the workload of tilling soil, a density of around 89 bulbs per m-2 would be optimal as it represents the best compromise between individual plant growth and division and plant yield per area.

Leaf Harvest

Although wild leek plants are usually harvested as whole plants, harvested leaves can be used fresh or prepared (e.g. pesto) in different culinary dishes (Facemire 2009). From the point of view of the plant, leaf harvest is much less destructive than bulb harvest, but can still affect carbon reserves and therefore bulb size if it occurs too early in the season as shown on onion (Muro et al. 1998). Removing leaves before senescence will also affect plant mineral nutrition status since many of the nutrients located in the leaves are massively translocated to the bulb during leaf senescence (Nault and Gagnon 1988; Rothstein and Zak 2001). We tested the impact of harvesting 50 or 100% of the leaves 15, 20 or 25 days after complete leaf unfolding on subsequent plant growth (Dion et al. 2016b). As expected, plants were less affected when only 50% of the leaves were removed than when all leaves were removed. Plant size, plant division and flowering were affected by leaf harvest. Wild leek plants were also less affected when leaf harvest occurred later in the season. According to these results, we would recommend harvesting half of the leaves 20 to 25 days after leaf unfolding, since plants were able to completely recover within a year or two. However, in a commercial situation, harvesting all leaves would be faster than harvesting half of the leaves on each plant. We thus recommend waiting until leaves of harvested plants have attained their pre-harvest size before subjecting them to another harvest. This might take two to four years depending on the conditions as warm or dry springs do negatively affect wild leek growth (Bernatchez et al. 2013).

Bulb Harvest

As plant density can attain high values in natural populations — 350 to 400 bulbs m-2 — we tested the impact of reducing the number of bulbs within a patch on subsequent plant growth (Dion et al. 2016b). All plants were dug out (plots of 100 mature plants) then either all were replanted (control plants to test the impact of digging on subsequent growth), or 20% or 40% of mid-size plants were harvested and the rest replanted. We also followed plots which were not dug out as a second control. Digging strongly affected plant size the following year as reported previously (Vasseur and Gagnon 1994). Digging out all bulbs is however the only efficient method in dense plots to select mid-size bulbs without damaging the large reproductive and small regenerating bulbs which are then replanted in order to favor recruitment from both bulb division and seedling establishment. All the chosen plots were high-density plots but due to large variation in plant density, there was an important overlap in terms of bulb density per plot following bulb harvest which potentially diminished the probability to detect differences among treatments. Two other factors complicate the analysis of such experimental design. Harvesting mid-size plants can influence the mean plant leaf size depending on the proportion of large and small plants in the plot. This can be corrected to some extent by estimating the mean leaf size in control plots after having removed from the data, 20 or 40% of the mid-size plants within these plots. Stochastic events also complicate the analyses. In this study, all plants reduced in size from year 3 to year 4 to the extent that plants were smaller in year 4 than in year 2. Nevertheless, the results suggest that plant growth rate was increased in plots subjected to partial bulb harvest compared to that of control (un-dug) plots. To lessen competition in dense plots would require reducing plant number down to 50 to 100 plants m-2 as shown in the Plant Density experiment (Dion et al. 2016b). The grower would need to wait until the plant density has attained high values again (over 200 plants m-2) before harvesting in the same plots; that could take many years due to the slow growth of the plant and to stochastic events.

Conclusions

These studies have allowed us to better define the conditions that improve wild leek growth under forest farming conditions at its northern limit of distribution, along with factors that will require further studies. Wild leek would benefit from being planted under late closing canopy such as under oak, ash or linden. The presence of a thick litter appears to improve growth, although further studies are needed to confirm these preliminary results and determine whether long-term exposure to the litter of some tree species such as that of walnut could be deleterious. Mineral fertilization improves plant growth but since an annual fertilization appears required, economical studies are needed to balance costs and benefits. Furthermore, micronutrients should be monitored as they could be limiting in some soils. Gypsum should be added in soils presenting low Ca level. We did not find any short time benefit to soil tilling, but this factor would need to be tested in different types of soils before drawing conclusions. We recommend a planting density of no more than 100 bulbs m-2, to avoid competition over time as bulbs get bigger and divide, but also to reduce the probability of infestation that can rapidly destroy the whole plot. Indeed, yearly monitoring of bulb mites and millipedes could prevent extensive damage. Leaf harvest is sustainable but should occur at least 20 days after complete leaf unfolding; furthermore, growers should wait until plants have reached pre-harvest size before harvesting the same plants again. Partial harvest of plants in very dense populations could improve subsequent growth of the remaining plants. However, partial harvesting in natural populations should only occur where the species is not endangered and these sites should then be left to recover their initial densities before another partial harvest is allowed.

References

Anderson R.C. (1994) Height of white-flowered trillium (Trillium grandiflorum) as an index of deer browsing intensity. Ecological Applications 4 (1): 104–109.

Badri M.A., Minchin P.E.H., Lapointe L. (2007) Effects of temperature on the growth of spring ephemerals: Crocus vernus (L.) Hill. Physiologia Plantarum 130: 67–76.

Bernatchez A., Lapointe L. (2012) Cooler temperatures favour growth of wild leek (Allium tricoccum), a deciduous forest spring ephemeral. Botany 90 (11): 1125–1132.

Bernatchez A., Bussières J., Lapointe L. (2013) Testing fertilizer, gypsum, planting season and varieties of wild leek (Allium tricoccum) in forest farming system. Agroforestry Systems 87 (5): 977–991.

Corio K., Wolf A., Draney M., Fewless G. (2009) Exotic earthworms of great lakes forests: a search for indicator plant species in maple forests. Forest Ecology and Management 258: 1059–1066.

Couillard L. (1995) La situation de l’ail des bois (Allium tricoccum) au Québec. Direction de la conservation et du patrimoine écologique, ministère de l’Environnement et de la Faune, Québec, Canada.

Dijkstra F.A. 2003. Calcium mineralization in the forest floor and surface soil beneath different tree species in the northeastern US. Forest Ecology and Management 175: 185–194.

Dion P.-P., Brisson J., Fontaine B., Lapointe L. (2016a) Light acclimation strategies change from summer green to spring ephemeral as wild-leek plants age. American Journal of Botany 103 (5): 963–970.

Dion P.-P., Bussières J., Lapointe L. (2016b) Sustainable leaf harvesting and effects of plant density on wild leek cultivation plots and natural stands in Southern Quebec, Canada. Agroforestry Systems 90 (6): 979–995.

Dion P.-P., Bussières J., Lapointe L. (2017) Late canopy closure delays senescence and promotes growth of a spring ephemeral, Allium tricoccum. Botany 95: 457–467.

Facemire G (2009) Having your ramps and eating them too. McClain Printing Company, Parsons, USA.

Gandin A., Gutjahr S., Dizengremel P., Lapointe L. (2011) Source-sink imbalance increases with growth temperature in the spring geophyte. Journal of Experimental Botany 62 (10): 3467–3479.

Kingery W.L., Wood C.W., Williams J.C. (1996) Tillage and amendment effects on soil carbon and nitrogen mineralization and phosphorus release. Soil and Tillage Research 37: 239–250.

Kristenen H.L., Debosz K., McCarty G.W. (2003) Short-term effects of tillage on mineralization of nitrogen and carbon in soil. Soil Biology and Biochemistry 35: 979–986.

Lapointe L., Lerat S. (2006) Annual growth of the spring ephemeral Erythronium americanum as a function of temperature and mycorrhizal status. Canadian Journal of Botany 84: 39–48.

Muro J., Irigoyen I., Lamsfus C. (1998) Effect of defoliation on onion crop yield. Scientia Horticulturae 77:1–10.

Nadeau I., Olivier A. (2003) Revue de la biologie et de la production du ginseng à cinq folioles (Panax quinquefolius L.) en milieu forestier au Canada. Canadian Journal of Plant Science 83:877–891.

Nault A., Gagnon D. (1988) Seasonal biomass and nutrient allocation patterns in wild leek (Allium tricoccum Ait.), a spring geophyte. Bulletin of the Torrey Botanical Club 115: 45–54.

Nault A., Gagnon D. (1993) Ramet demography of Allium tricoccum, a spring ephemeral, perennial forest herb. Journal of Ecology 81:101–119.

Nantel P., Gagnon D., Nault A. (1996) Population viability analysis of American ginseng and wild leek harvested in stochastic environments. Conservation Biology 10:608–621.

Neufeld H.S., Young D.R. (2014) Ecophysiology of the herbaceous layer in temperature deciduous forests. In: Gilliam F.S. (ed) The herbaceous layer in forests of Eastern North America, 2nd ed. Oxford University Press, New York, USA, pp 35–95.

Persons W.S., Davis J.M. (2005) Growing and marketing ginseng, goldenseal and other woodland medicinals. Bright Mountain Books, Fairview, USA.

Ritchey K.D., Schumann C.M. (2005) Response of woodland planted ramps to surface-applied calcium, planting density, and bulb preparation. HortScience 40:1516–1520.

Rock J.H., Beckage B., Gross L.J. (2004) Population recovery following differential harvesting of Allium tricoccum Ait. in the southern Appalachians. Biological Conservation 116:227–234.

Rothstein D.E., Zak D.R. (2001) Relationships between plant nitrogen economy and life history in three deciduous-forest herbs. Journal of Ecology 89:385–394

Rousseau C. (1974) Géographie floristique du Québec-Labrador. Distribution des principales espèces vasculaires. Les Presses de l’Université Laval, Québec, Canada.

Routhier M.-C., Lapointe L. (2002). Impact of tree leaf phenology on growth rates and reproduction in the spring flowering species, Trillium erectum (Liliaceae). American Journal of Botany 89: 500–505.

Vasseur L., Gagnon D. (1994) Survival and growth of Allium tricoccum Ait. transplants in different habitats. Biological Conservation 68:107–114.