Competition between plants for light, water and nutrients is one of the most powerful biotic interactions in nature and, as such, influences individuals, populations [1
], communities [2
] and, hence, ecosystem dynamics and evolution [3
]. Competition may be a strong determinant of patterns of natural regeneration in plant communities; e.g., the natural or man-made removal of dominant individuals may release seedlings from competitive stress [4
]. The intricacies underlying the basic mechanisms and ecological consequences of competition is thus of key importance in the management of various socioeconomically important ecosystems. For example, the development of forest management practices, including an uninterrupted maintenance of forest cover (i.e
., continuous cover forestry) requires seedlings to establish under a semi-closed canopy and, so, in competition with dominant trees.
The relative effects of above- and below-ground competition may have an important influence on seedling recruitment under canopy trees [6
]. The theory of multiple resource limitation predicts that seedling performance will depend on the availability of water and nutrients, as well as on the shading properties of the canopy formed by the overstory [8
]. Theories of asymmetric competition suggest that understory plants (such as seedlings establishing beneath closed canopies) may be particularly sensitive towards competition for light, as this resource can be pre-emptied by dominant vegetation [9
]. Based on a review of trenching experiments, Coomes and Grubb [10
] proposed some general hypotheses, e.g., that light alone limits seedling growth in forests on moist, nutrient-rich soils, but that competition for belowground resources is more important on infertile soils and in drier regions. Early observations from the pine-dominated forest ecosystem of boreal Fennoscandia suggested that competition was fundamentally important, and many early researchers argued that belowground competition should be the most important factor in these systems [11
]. Although some recent researchers agree with this notion [14
], others have suggested that light is the most essential factor affecting the establishment and growth of pine seedlings [15
]. However, studies on belowground competition are still under-represented in the literature, and empirical knowledge is consequently limited [10
]; but, see, for example, Petritan et al.
The regeneration of Scots pine (Pinus sylvestris
L.) seedlings in the pine-dominated forest ecosystems of boreal Eurasia was already of interest 100 years ago; see, for example, [6
]. Reduced regenerative growth of pine seedlings along edges or in the vicinity of retention trees is a commonly described pattern in boreal pine forest [11
], and early research concluded that gaps within the forest should exceed a certain size in order to allow sufficient seedling establishment. Consequently, leaving seed-trees on relatively large clear-cuts has been the preferred method to foresee sufficient plant establishments. However, with the reconsideration of alternative forest practices, such as continuous cover forestry, the competitive mechanisms of importance for seedling establishment are in need of further examination. This is important not only in commercial forestry, but also in the restoration and conservation of remnant pine forests in, for example, Scotland [23
In the present paper, we present results from two separate studies on seedling establishment in nutrient-poor pine forests typical of the northern boreal region of Fennoscandia. Our aim was to address the roles of aboveground competition for light and belowground competition for nutrients for pine seedling establishment beneath tree canopies. In the first study, we investigated the temporal patterns of pine seedling establishment following the stem-girdling of dominant trees performed 12 years earlier. Stem-girdling is a novel approach to disconnect, in the short-term (i.e
., as long as the tree canopy remains intact), the influence of aboveground and belowground competition on seedling establishment. This method of interfering with belowground competition avoids a number of artifacts arising when more destructive techniques are used, such as soil trenching, which alters moisture and directly severs the structural integrity of roots and fungal hyphae. Earlier studies have shown that girdling instantaneously terminates the flux of photosynthates (sugars) from the tree canopy, via the phloem, to the roots and associated mycorrhizal fungi, while it initially allows the upward transport of water through the xylem [25
]. Hence, during the two years following girdling, seedlings establishing beneath the canopy will be exposed to the same aboveground shading as before girdling (or on non-girdled control plots), while the belowground competition will be relaxed due to the lowering of nutrient uptake capacity by tree roots and their associated mycorrhizal fungi. This first study goes beyond the earlier initial studies on soil processes [25
] to investigate if the relaxation of belowground competition with canopy trees can have long-term effects on pine seedling establishment and growth. In the second study, we explored the influence of being released from both above- and below-ground competition at forest edges on the pattern of pine seedling establishment. Previous studies from pine-dominated forests in other parts of the boreal region have demonstrated that across forest edges towards gaps, an approximately 10 m-wide zone occurs, in which pine-seedling establishment and growth is poor, while beyond that zone, pine regeneration becomes denser [11
]. In the present study, we contrast seedling establishment and growth across forest edges facing either north or south to test for any effects due to differences relating to the amount of solar radiation received by regenerating seedlings. We also conducted surveys on understory vegetation to explore correlations between pine seedling regeneration and the abundance of different understory plant species.
Our results demonstrate that pine seedling establishment and growth in nutrient-poor boreal pine forests can be successful under a canopy of dominant trees, given that belowground competition with overstory trees is disrupted. Disrupting the belowground competition, while at the same time retaining the shading properties of the overstory canopy, resulted in the establishment of nearly 22,000 pine seedlings ha−1
during a two-year period, which is more than sufficient for normal stand development. The disruption of belowground competition may be attributed to competition for both water and nutrients and is likely to involve soil-associated microbes, such as ectomycorrhizal fungi. However, girdling initially does not affect the upward transport of water through the xylem [25
]. The needles that remain in the canopy drive the water transport, and girdled trees should thus maintain their competitive ability for water as long as the canopy is intact. This is supported by Bhupinderpal-Singh et al.
], who reported from the same study site that soil moisture during the first years after girdling did not differ between girdled and un-girdled plots. In contrast, the terminal effect of girdling on photosynthate transport from the tree canopy to the roots was instantaneous and pronounced. Previous reports from the same study site have shown that the termination of the downward photosynthate flow induced by stem-girdling of the dominant trees resulted in the soil microbial biomass being reduced by one-third within 1–3 months due to the loss of the extra-matrical mycelium of ectomycorrhizal fungi [27
]. Thus, the establishment and growth of pine seedlings was clearly promoted by disrupting the interaction between the dominant trees and their ectomycorrhizal fungi, hence reducing the competitive ability of the dominant trees for available nutrients. Moreover, nitrogen locked in ectomycorrhizal mycelia, which were made available by decomposition, may have further promoted pine seedling development. The loss of ectomycorrhizal mycelial biomass during the three-month period following girdling was estimated to be equivalent to ca
. 60 kg∙ha−1
of carbon and approximately 6 kg∙ha−1
of nitrogen [27
]. An analysis of the isotopic composition of nitrogen in leaves of understory dwarf-shrubs, one year after girdling, suggested that nitrogen released from ectomycorrhizal mycelium became available for plant uptake at the time of pine seedling establishment after girdling [26
]. However, the amount of soil nitrogen normally taken up by canopy trees in this type of forest is far higher [37
] than the nitrogen potentially gained from the decomposition of mycelium. Hence, the main beneficial effect of tree girdling on seedling establishment at this stage is likely to be competitive release from the dominant trees and their associated microorganisms and not increased nitrogen availability.
In the third growing season following the girdling, the trees started to shed their needles [26
], and their subsequent decomposition fertilized the site. Hence, while the aboveground competition for light was diminished beneath the tree canopy, nitrogen availability increased. Our estimations suggests that the trees shed approximately 6000 kg–7000 kg of needle biomass ha−1
, which should contain approximately 50 kg–70 kg of nitrogen, of which about 50% may be released over the course of a few years. The relaxation of aboveground competition while the availability of nitrogen increased correlated with the establishment of the majority of pine seedlings (ca
. 50,000 ha−1
) that were still present on the plots 12 years after tree girdling.
We also studied pine seedling establishment and growth in forest gaps caused by clear-cutting confirming the conclusion from the girdling study that belowground competition is a main driver of pine seedling establishment and growth in boreal pine forests. Our result confirmed patterns of pine seedling establishment and growth previously observed in similar pine-dominated ecosystems in northern Finland nearly a century ago by Aaltonen [11
] and later revisited by Kuuluvainen and Yllasjarvi [20
]: that pine seedlings in the central areas of gaps grew better than seedlings closer to forest edges and that along the edges, there were 5 to 10 m-wide zones in which there were about the same number of seedlings as there were further away from the edge, but which were growing relatively poorly. In an earlier study at our site, Göttlicher et al.
] used two different methods, e.g., counting ectomycorrhizal sporocarps and 15
N labeling, to estimate that the lateral spread of tree roots from tree trunks was about 4–5 m. Our observation of a 5 to 10 m-wide zone with relatively poor pine seedling growth suggests that the distance influenced by belowground competition from a dominant tree may be slightly greater than the 4 to 5 m estimated by Göttlicher et al.
]. However, the experimental study by Göttlicher et al.
] was done within a few years following edge formation, whereas this study and the study by Aaltonen [11
] were made along forest edges formed more than 10 years prior to the studies. It is plausible that dominant trees along forest edges expand their root systems into a gap over time to exploit any belowground resources being mobilized there.
In our comparison of north-facing and south-facing forest edges, we found that there were twice as many seedlings along edges with a northerly aspect than there were along edges facing south, while aspect had no effect on seedling height. This result contradicts those of previous studies in boreal forests, where a positive relation between seedling growth and incoming radiation has usually been indicated [15
], although some negative or non-significant relationships have also been reported [12
]. We agree with previous authors who point out that observational studies are of limited use when trying to evaluate the importance of radiation for seedling establishment and growth, since in these situations, radiation cannot be separated from belowground competitive interactions [17
]. Nevertheless, a lack of clear positive effect on seedling growth in south-facing edges suggests that even quite high light levels are not enough to compensate for the depressing influence of canopy trees. Thus, the patterns of seedling establishment in the girdled forests should mainly be due to release from belowground competition and not over light. Moreover, in our study system, the larger number of seedlings found along north-facing forest edges may be due to more favorable abiotic conditions for seedling establishment, such as a higher supply of moisture and less extreme variations in temperature than along south-facing forest edges. Such differences in abiotic conditions are also indicated by the observed differences in the composition, dominance and diversity of other plant species growing on north- and south-facing forest edges. For example, moisture-demanding mosses were more abundant in gaps along north-facing edges, whereas drought-tolerant lichens dominated the bottom-layer vegetation in gaps along south-facing edges.
It has been suggested that interactions between tree seedlings and ground vegetation may influence seedling establishment [6
]. Along the forest-to-gap transects, the ground vegetation underwent distinct compositional changes. Lichens and mosses replaced each other, with mosses dominating the bottom-layer vegetation in the forest, whereas lichens dominated in the gaps, particularly along south-facing forest edges. It has been suggested that pine seedling establishment in northern boreal pine forests is more successful on lichen-dominated microsites than on moss-dominated microsites [40
]. In contrast, we found that the numbers of pine seedlings in gaps were significantly higher along north-facing edges, where mosses were more abundant, than along south-facing forest edges, where lichens were more abundant. Moreover, obviously the species composition of the understory vegetation reflects the environmental conditions of the site. As the same environmental conditions affecting ground vegetation also affect the tree seedlings, the mechanisms of cause and effect underlying the observed correlations between understory species composition and tree seedling establishment and growth are difficult to disentangle. It is, however, clear that the role of the understory vegetation for pine seedling establishment and growth is subordinate to the role of competition from dominant trees. Whereas shifts in understory species composition occurred sharply at the forest edge along the forest-to-gap transects, seedling growth was suppressed in gaps in a 5–10 m-wide zone along the edge.
Our results have clear implications for the practice of continuous cover forestry with single-tree selection cuttings. In such practices, the spacing between trees will determine the size of gaps created after harvest. Our data suggest that in this nutrient-poor ecosystem, the spacing between trees may need to be as large as 10 m × 10 m in order to ensure a sufficient tree replacement, thus restricting the number of stems to approximately 100 trees ha−1
. This is in agreement with empirical studies of the natural regeneration of pine on similar sites where the number of seed-trees per hectare often is recommended to be less than 100–150 ha−1
to ensure that the seed-trees do not adversely affect the regeneration [39