Next Article in Journal
Phylogenomic Reconstruction of the Neotropical Poison Frogs (Dendrobatidae) and Their Conservation
Previous Article in Journal
Movement and Home Range of the Smooth Softshell Turtle (Apalone mutica): Spatial Ecology of a River Specialist
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Diversity
Volume 11
Issue 8
10.3390/d11080125
diversity-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Willow Short-Rotation Coppice as Model System for Exploring Ecological Theory on Biodiversity–Ecosystem Function

by
Martin Weih
1,*,
Carolyn Glynn
1 and
Christel Baum
2
1
Department of Crop Production Ecology, Swedish University of Agricultural Sciences, 75007 Uppsala, Sweden
2
Soil Science, Faculty of Agricultural and Environmental Sciences, University of Rostock, 18059 Rostock, Germany
*
Author to whom correspondence should be addressed.
Diversity 2019, 11(8), 125; https://doi.org/10.3390/d11080125
Submission received: 19 June 2019 / Revised: 18 July 2019 / Accepted: 25 July 2019 / Published: 29 July 2019
(This article belongs to the Special Issue Biodiversity of Short Rotation Willow and Perennial Rhizomatous Grass Crops)
Browse Figures
Versions Notes

Abstract

:
Plantations of willow (Salix spp.) are today grown as short-rotation coppice (SRC) for the sustainable production of biomass. While developing these production systems in the past, much ecological knowledge on plant–plant, plant–environment and trophic interactions has been generated. This knowledge can contribute to the further development of biodiversity–ecosystem function (BEF) theory, which frequently lacks a sound understanding of the complex mechanisms behind the observed patterns of diversity-productivity relationships. Thus, willow SRC systems are suitable models to explore BEF theory; they are simple enough to allow the study of the complex ecological mechanisms involved and they have many similarities to grassland systems in which much of recent BEF theory development has been achieved. This paper briefly reviews the current observational and mechanistic knowledge on diversity–productivity relationships in willow SRC, as well as the most important above- and below-ground trophic interactions that are likely to affect them. If the available knowledge is integrated and combined with further experimental work targeting mechanisms behind patterns, research on willow SRC as a model offers a great opportunity for filling the gaps in the understanding what presently hampers the development of predictive BEF theory.

Graphical Abstract

1. Introduction

Willows (genus Salix, family Salicaceae) are fast-growing deciduous trees and shrubs occurring mostly in temperate and arctic zones of the northern hemisphere [1]. Intensively managed willow plantations are commercially grown for biomass production in many regions of the world, and the short-rotation coppice (SRC) systems most often used are gaining interest worldwide mainly due to their efficient and sustainable land use along with an increasing demand for biomass resources [2]. Willow SRC plantations consist of densely grown (10,000 to 20,000 plants ha−1), high-yielding genotypes of willow cultivated on agricultural land; and the shoots are typically harvested during winter for biomass on the basis of two- to five-year cutting cycles [3]. The rootstock remains in the ground after each shoot harvest, with new shoots re-sprouting the following spring. Thus, in an ecosystem function perspective, the regular shoot harvests every second to fifth year allow for the study of temporal patterns in shorter (two to five years) and longer time scales (>five years). Additionally, the controlled removal of above-ground plant parts while rootstock is sustained implies that competitive exclusion and extinction of individual genotypes is reduced. In the cases where several genotypes are grown in the same plantation, willow SRC systems, with the above characteristics, are attractive for the study of diversity–productivity relationships and the development of (predictive) biodiversity–ecosystem function (BEF) theory. This is supported by the high level of functional diversity present across the various species and genotypes used in willow SRC systems as evidenced by the results from controlled pot experiments, (e.g., [4,5,6,7]), and experimental field trials (Table 1).
Originally initiated by a number of influential ecosystem studies carried out in grasslands, it has more recently been reported in a broad range of ecosystems worldwide that greater species diversity increases productivity [11,12]. However, generalizations have not been forthcoming due to conflicting interpretations of the same results [13], high complexity of the processes involved, and to an associated lack of predictive BEF theory especially when several trophic levels are taken into consideration [14]. Importantly, investigators have focused more often on the consequences of interspecific diversity for plant growth and productivity, involving the use of taxonomic predictors of diversity, rather than on the functional mechanisms behind observed patterns. For example, it is unclear which genetically-based differences in plant phenotype, and under which environmental conditions, result in differential niche occupation and thereby significantly contribute to diversity–productivity relationships; and which trait differences (or combinations) are unaccompanied by strong differences in resource use and therefore result in similar niche occupation (with no diversity–productivity effects realized). In addition, theoretical approaches based on the functional traits of the involved species or genotypes are beginning to replace studies based upon taxonomic predictors [15]; they are however challenging. This is because functional traits may influence processes at different levels of organization (e.g., trophic levels), at different time scales, and as such their influence may change over time [15]. For example, mixtures of species (or genotypes) with contrasting traits could use resources more effectively and reduce losses, but the positive effects may depend on the characteristics of the mixture components and the environmental conditions (e.g., resource availability), and change over time.
By linking emerging knowledge on plant functional traits, plant diversity and ecosystem processes at several trophic levels, BEF theory could be further developed with regard to a better understanding of the underlying mechanisms and their interactions (Figure 1). Examples of this are previous works in willow SRC that have focused on plant functional traits in relation to environment [8,16,17,18], plant interactions with insect herbivores and root-associated fungi [6,7,19,20], and plant–plant interactions [21]. This review briefly summarizes some of the current knowledge on willow SRC research that is relevant for BEF theory development in terms of diversity effects on growth and productivity, and the associated trophic interactions above- as well as below-ground. Consideration of other trophic levels in addition to producers is important, not least because individual ecosystem processes can be more strongly affected by the overall diversity of functional traits and the diversity of microorganisms influencing decomposition and nutrient cycling, than by tree species richness [22].

2. Tree Diversity and Productivity

The commercial SRC cultivation practice is based on intensive management actions including weed control [2]. On the one hand, the weed control strategy strongly affects the establishment, development and biomass productivity of the main crop in willow SRC systems [24,25]; suggesting SRC systems to be grown with a minimum of ground vegetation in order to maximize biomass productivity. On the other hand, plantations of willow SRC grown on agricultural land often have greater plant diversity compared to stands of cereals, spruce and fallow ground, for example [26,27], suggesting a hitherto unexplored opportunity that a diverse ground vegetation could benefit biogeochemical cycling and productivity. With regard to the main crop, most commercial willow SRC grown for biomass production currently consist of single species or genotypes. Apart from the environmental (climate, soil) and management conditions, the growth and productivity in willow SRC are strongly affected by the specific characteristics of the plant material used in the plantation (Figure 1). Instead of growing pure stands, the cultivation of mixed stands including fast-growing components (species or genotypes) could be one way to enhance stand growth by making use of selection effects according to BEF theory [11]. Already early theoretical ecological frameworks [28,29] suggested that the more complex ecosystems become in terms of their food webs, the more efficient they are in utilizing resources, and a corollary of this is that enhanced biodiversity would improve biogeochemical cycling and productivity [11,30]. Observational studies in differently-composed tree stands suggest indeed that the composition of a plantation in terms of pure stands, consisting of single species or genotypes, or mixed stands can positively affect productivity [31,32]. Several mechanisms have been invoked to explain why biodiversity can have such a positive effect on productivity [11,33], but a clear understanding of the mechanisms underpinning BEF is still missing [14,34,35]. In willows, the effect of species or genotype mixture on growth was explored in a controlled growth container study in which plants were cultivated in two environments differing in resource (nutrient) supply [36]. This study demonstrated that the specific functional trait combinations of two individual species/genotypes affect their response to mixture as compared to pure culture; and the results support the hypothesis that mixtures perform equally well or better than pure cultures especially in low-resources environments. In field-grown stands, no clear evidence has been found so far for a strong positive effect of stand diversity on productivity in young willow SRC [21,37], but it is possible that a (positive) diversity effect on productivity will evolve as these plantations grow older. Despite of the absence of a clear diversity effect on stand productivity after three years of growth, it was demonstrated that the addition of two of the genotypes (‘Jorr’ and ‘Loden’) resulted in enhanced community biomass production, while others (‘Tora’ and ‘Björn’) were found to reduce community biomass production in the mixed stands [21]. In terms of BEF, evidence was found for a negative selection effect due to the genotype ‘Tora’ performing better in mixed than in pure communities in two of the experimental sites (Freiburg, Uppsala) [21]. The results imply that increasing genetic richness has no significant effect on community productivity during the first three years of growth; and provide evidence that specific functional trait combinations of individual genotypes affect community productivity in either a positive or a negative direction. The trait profiles of the individual genotypes used in these trials, along with their temporal trajectories, may be further explored and linked to the genotype-specific effects on community productivity (e.g., Figure 2). The generated knowledge could then be used to test general predictions of BEF theory, especially when additional data on processes including more than one trophic level are considered [14]. For example, the corresponding work could be done in the willow SRC trials previously discussed [21], as these are part of the TreeDivNet network, which is the largest network of biodiversity experiments worldwide and provides a unique platform for BEF related research in a global perspective [32].

3. Tree Diversity and Above-Ground Trophic Interactions

With regard to further theory development of BEF and the questions of if and how genotype and species diversity affect ecosystem functions, diversity experiments have investigated how plant performance (growth and survival) and their vulnerability to herbivory or rust infestation are affected by community diversity [35,38,39,40] (Figure 2). In this context, community diversity is increasingly acknowledged to provide associational resistance to herbivores and rust infestation; lower levels of herbivory and rust disease have been found in mixed than in mono-specific plots [41,42]. However, the opposite—associational susceptibility—can also occur [43,44].
The example of associational effects, which classically results from both bottom-up and top-down processes (e.g., Figure 2), illustrates the point that improved understanding of BEF requires the development of predictive models that accommodate both of these essential processes. In this context, willow SRC systems are excellent model systems, because they provide these.
Work done on BEF to date reveals no conclusive patterns with regard to how above ground trophic interactions respond to the genetic diversity of plant communities. Much of the data generated on this issue is conservation oriented and reported from wild populations, yet production-oriented cropping systems also play an increasingly important source of data [45]. This is driven by the demand for reduced utilization of chemical pesticides and fungicides, and an increasing awareness of the importance of biodiversity and ecosystem functions in production systems [46]. A recently published meta-analysis of 60 experimental studies on arthropods illustrates some of the complexities of relating stand genetic diversity with herbivore damage [47]. The results from that analysis lead to a few general conclusions: Both insect herbivores and their predators were higher in diverse wild plant communities, and herbivore abundance was lower in cropping systems that had higher crop genetic diversity, yet predator abundance was not affected there. One crucial factor to take into account is if the herbivores are generalists or specialists on their host plants. The meta-analysis [47] revealed that damage caused by generalists was lower in diverse systems and that specialist herbivores were unaffected. In short, it was concluded that plant genetic diversity does indeed affect arthropod communities (both herbivores and predators) yet there is limited potential for the use of crop mixtures as a means of pest control in agricultural systems [47].
These reported patterns are important advances; however, the mechanisms underlying the variability in results are yet to be discovered. This makes for a limited predictive power as BEF stands today. Willow systems, and especially those related to SRC, allow for rigorous tests of BEF theory development with regard to aboveground trophic interactions in production systems. In particular, they can play an instrumental role in identifying key components that link plant diversity levels and damage caused by herbivores that are useful for generalizations regarding both production and conservation systems. Further, mixed stands of SRC willow could provide suitable test systems for the adaptation and durability of rust resistance in the light of BEF theory, which also is an important research subject in plant pathology [38]. Willow SRC models allow for investigations that standardize many elements (genetic stand composition, soil nutrient status, levels of biotic influence, harvest regime) so that the effects of one or a few factors can be addressed in a specific experiment.
Over time, research efforts based upon willow model systems have led to emerging patterns on an array of abiotic and biotic factors affecting willow–pest interactions including at least two trophic levels. The reported interactions often address insect herbivores [6,41,48,49,50,51,52,53,54,55], but also fungal and bacterial diseases [39,40] or mammalian herbivores [56]. Other studies accommodate a third trophic level and give insights into how plant (willow) community structure affects the natural enemy pressures on herbivores [20,53,57,58,59]. The abiotic factors considered include mostly soil nutrient status [54] and water regime [6,60]. While no conclusive general principles can be made on how biotic and abiotic factors affect willow–pest interactions, a few patterns can be noted from the studies mentioned above. There is genetically-based variability in many willow interactions including several trophic levels: resistance to fungal and bacterial diseases, susceptibility to insect and mammalian herbivores, resistance to certain insect herbivores, production of a variety of secondary metabolites that serve as defense against herbivores and pathogens, soil nutrient status and water regimes. The variability in these traits, coupled with the ease of establishing structured experiments based on willows, allows for a uniquely mechanistic approach to theory building within the BEF framework and the questions of if and how genotype and species diversity affect ecosystem functions that are realized through the integration of processes at several trophic levels.

4. Tree Diversity and Below-Ground Trophic Interactions

Soil microbial communities, of which mycorrhizal fungi are an integral component, are important controls of soil health and plant productivity in ecosystems [61]. Salix spp. belong to the low number of dual-mycorrhizal plants forming both arbuscular and ectomycorrhizal symbiosis. For this reason they were used as model organisms, for the evaluation of the specific benefits of fungal diversity in plant nutrition and biomass production [62] (Figure 2). In general, mycorrhizal fungi regulate nutrient transfer between plants and soil via mycelial networks [63], and the utilization of mycorrhizal networks for influencing sustainability and productivity in biomass production systems such as willow SRC has been proposed [64,65]. Mycorrhizal networks are supported by plant-derived carbon, and increases in plant diversity have been associated with increased carbon storage in grassland [66] and forest soils [67]; however, the mechanisms behind are unclear. In most systems, mycorrhizal fungi receive 10 to 50% of plant-fixed carbon [68], and mycorrhizal fungal necromass constitutes an important pathway of carbon into long-term soil pools [69]. The quantity and composition of the microbial-mediated carbon flow from plant to soil depend on the functional traits of the microbial species involved [70], and the mycorrhizal fungal community composition is one of the main drivers of carbon and nutrient cycling in many soils (e.g., [71]). It has indeed been suggested to consider the quantity and quality of plant species-specific root colonization with mycorrhiza as plant traits for exploring patterns of soil carbon cycling [72]. Apart from mycorrhiza, it has been shown that the total soil microbial community composition—including both symbiotic and saprotrophic fungal and bacterial communities—reflects the quality of soil organic matter (SOM) so accurately that the soil microbial community may be used to predict SOM quality [73]. The SOM quality strongly affects its decomposition, and is therefore critical for the longevity and sustainability of the carbon pool accumulating in soil [73]. Hence, plant trait diversity potentially affects both quantity and quality of the carbon flow from above to below ground as well as the longer-term sustainability of the soil carbon pool.
In willows, the identity of the mycorrhizal partner has been shown to significantly influence the uptake of various nutrient elements, among them nitrogen and phosphorus, into the host plants [19,74], pointing at a strong influence of these fungi on the below-ground trophic interactions related to the productivity and function of these ecosystems (Figure 2). Arbuscular mycorrhizal fungi increased the stem phosphorus content of willows in vegetation filter systems up to 33% [75]. In addition, the diversity and abundance of root-associated fungi also affect the chemical composition of the foliage and consequently the above-ground trophic interactions related to the plants’ predisposition to herbivore attacks and infection by pathogens, like rust fungi [7,19] (Figure 2). Conversely, both the willow genotype identity and the length of the rotation period (cutting cycle) have been shown to affect the diversity of mycorrhizal fungi or saprophytic microorganisms under willow SRC, along with the activity of hydrolytic enzymes affecting nutrient cycling [76,77]. Although the diversity of ectomycorrhizal fungi in planted willow SRC has been found to be lower compared to adjacent natural willow stands [78], willow SRC was concluded to enrich the biodiversity of soils when compared to conventional agriculture-dominated landscapes, and the ectomycorrhizal fungi contribute considerably to that enrichment [79].
In spite of the many observational studies demonstrating patterns of functional relationships with regard to below-ground trophic interactions affecting BEF, quantitative investigations of the functional interactions between willow diversity, soil microbiology and nutrient cycling are rare. In a study with focus on the plant–soil interactions in willow SRC, mixing of genotypes with strong eco-physiological differences was hypothesized to change the diversity and abundance of root-associated fungi and phosphorus mobilization in the mycorrhizosphere, based on different expressions of root traits [80]. A most interesting result was that interspecific root competition increased the richness and root colonization by endophytic fungi more than by ectomycorrhizal fungi; and also increased the activities of hydrolytic soil enzymes involved in the phosphorus mineralization. This suggests a selective promotion of endophytic root colonization and changed competition for nutrients by mixtures of Salix genotypes compared to the pure cultures. These results indicate that the specific suite of traits in mixtures have significant effects on the soil processes related to phosphorus cycling, which are not committed by the pure cultures of the individual genotypes.
Based on their no-till management, willows grown in SRC also promote the soil faunal abundance and diversity, and thereby, the soil food web relating to below ground trophic interactions [65]. Thus, the soil fauna plays a pivotal but little understood role in both carbon and nutrient cycling. For example, in a comparison of different ecosystem types, the divergence of feeding channels within the soil food web was investigated using willows [81], and the willow system was identified as an appropriate model system for the exploration of BEF theory, linking the abundance of herbivores, microbivores, micropredators, omnivores and macro-predators with soil carbon and nitrogen cycling. In a recent review on the relationship between below-ground biodiversity and ecosystem services across European forests, soil biodiversity was concluded to be generally positively related to ecosystem services, but the authors identified huge knowledge gaps regarding especially the functional relationships between the diversity of soil biota and ecosystem services [82]. Willow SRC systems are promising models for performing research to close some of those knowledge gaps, not least because much knowledge is already available in these systems on the functional relationships relevant for BEF and the integration of various trophic levels.

5. Discussion and Conclusions

Much work has been already done on diversity–productivity relationships and BEF theory development, based mostly on observational investigations in grassland and forest systems. Even if we are rapidly gaining insights into the ecological and plant physiological interactions that affect production systems, we are far from able to predict them only by means of manipulating community structures. In addition, much of the research on diversity–productivity relationships was indeed focused towards the study of the consequences of interspecific diversity for plant productivity. The approaches using taxonomic predictors are less promising when using willow SRC, because the plant material used in this production system is usually taxonomically diverse and most often includes hybrid varieties with elements from various taxonomic entities or species [83]. Instead of using taxonomic predictors, approaches based on the functional traits of the involved species or genotypes seem more promising for exploring the mechanistic links between plant functional traits (or trait differences) and resource use or niche occupation, for example. There are, however, challenges as the functional traits of interest may influence processes at various trophic levels and their influence may even vary over time [14,15]. The willow SRC production system is based upon individual genotypes of known genetic pedigree that can be vegetatively propagated. In addition, much information is already available on the impact of abiotic factors such as water and nutrient (mostly nitrogen) supply on the growth of different willow genotypes [4,16,17,84]. This allows for a multidisciplinary approach where the role of fundamental attributes of individual willow genotypes (such as physiological growth traits, phytochemical production related to pest resistance, ability to compete with other plants) can be assessed in a community and ecosystem approach. As the previous sections have shown, for willow SRC much evidence is already available on the relationships between plant functional traits and the processes important (e.g., resource use), and this information includes processes at various trophic levels (Figure 2). Significant advances in the development of BEF theory that take into consideration both above and below ground trophic interactions can therefore be made by using willow SRC as model systems. For example, genotype by environment interactions can be stringently tested since willow genotypes and species are easily propagated and subjected to various abiotic and biotic treatments in field and laboratory situations. Apart from BEF theory development, results from such studies can also provide the basis for long-term plant production strategies that can increase plant resistance to pests and diseases and promote sustainable plant production methods (e.g., for producing biomass for biofuel use [2]).
There are many arguments underpinning the notion that willow SRC plantations are suitable model systems to explore BEF theory:
  • Willows are perennial and fast-growing.
  • Willow genotypes are easily cloned, reducing a source of variation in the system.
  • Willows are dual mycorrhizal (i.e., associated with arbuscular and ectomycorrhizal fungi), providing the consideration of both partly contrary impacts of the two main types of mycorrhiza formation on carbon cycling.
  • Willows promote the soil faunal abundance and diversity and are appropriate model systems for the investigation of the soil food web based on their no-till management.
  • Well-established field and greenhouse experimental willow model systems with varying levels of genotypic diversity are already part of professional biodiversity networks [32].
  • Regular shoot harvests allow for the study of temporal patterns in shorter (i.e., within one cutting cycle of three-year) and longer time scales (i.e., across subsequent cutting cycles).
  • Short-rotation willow systems have characteristics that are similar in functionality to other perennial systems such as grasslands, for which much of the relevant BEF theory development has been achieved.
  • The short-rotation practice of controlled removal of above ground plant parts while below ground parts are sustained implies low risk for competitive exclusion and extinction of genotypes, and thereby enhanced opportunities for the study of the mechanisms underlying plant–plant and plant–environment (abiotic and biotic) interactions in a BEF context.
In addition, major advances in BEF theory development hitherto came from experimental and modelling work done on diversity–productivity interactions in microbial and on grassland communities [85,86], which are species-rich systems. With so many species interactions, variability can be difficult to explore, although statistical models have been developed to address their complexity [87,88,89]. We suggest that the simplicity of the willow SRC system in itself contributes to and complements advancements in BEF theory; it allows for species interactions to be stringently manipulated experimentally and assessed. By working with willow SRC systems of fewer species, interactions of biological importance that occur across trophic levels could be revealed.
Due to the various advantages mentioned, and the notion that willow SRC systems seem to be simple enough to allow the study of the complex mechanisms involved in plant–plant and plant–environment (abiotic and biotic) interactions in a BEF context, we consider this model system attractive for future research that could fill the gaps in our understanding of what presently hampers the development of predictive BEF theory.

Author Contributions

M.W. initiated the manuscript and had overall responsibility for the literature compilation and writing; C.G. and C.B. were mainly responsible for the parts of the text related to above-ground trophic interactions (C.G.) and below-ground trophic interactions (C.B.), and also contributed substantially to review and edit the manuscript.

Funding

This research was partly funded by a grant from the Swedish research council Formas to Stefano Manzoni and M.W., grant number 2016-00998.

Acknowledgments

We are very grateful especially to S. Hoeber, P. Fransson and N.-E. Nordh, who partly carried out or otherwise greatly supported much of the research reviewed here.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Dickmann, D.I.; Kuzovkina, J. Poplars and Willows of the World, With Emphasis on Silviculturally Important Species. In Poplars and Willows: Trees for Society and the Environment; Isebrands, J.G., Richardson, J., Eds.; Cabi Publishing: Wallingford, UK, 2014; pp. 8–91. [Google Scholar]
  2. Weih, M.; Hansson, P.A.; Ohlsson, J.A.; Sandgren, M.; Schnürer, A.; Rönnberg-Wästljung, A.C. Sustainable willow production for biofuel use. In Achieving Carbon-Negative Bioenergy Systems from Plant Materials; Saffron, C., Ed.; Burleigh Dodds Science Publishing Limited: Cambridge, UK, 2019; ISBN 978-1-78676-2528. in press. [Google Scholar]
  3. Larsson, S.; Nordh, N.E.; Farrell, J.; Tweddle, P. Manual for SRC Willow Growers; Lantmännen Agroenergi AB: Örebro, Sweden, 2007; p. 18. [Google Scholar]
  4. Weih, M. Evidence for increased sensitivity to nutrient and water stress in a fast-growing hybrid willow compared with a natural willow clone. Tree Physiol. 2001, 21, 1141–1148. [Google Scholar] [CrossRef] [PubMed]
  5. Weih, M.; Nordh, N.E. Characterising willows for biomass and phytoremediation: Growth, nitrogen and water use of 14 willow clones under different irrigation and fertilisation regimes. Biomass Bioenergy 2002, 23, 397–413. [Google Scholar] [CrossRef]
  6. Glynn, C.; Ronnberg-Wastljung, A.; Julkunen-Tiitto, R.; Weih, M. Willow genotype, but not drought treatment, affects foliar phenolic concentrations and leaf-beetle resistance. Entomol. Exp. Appl. 2004, 113, 1–14. [Google Scholar] [CrossRef]
  7. Baum, C.; Toljander, Y.K.; Eckhardt, K.-U.; Weih, M. The significance of host-fungus combinations in ectomycorrhizal symbioses for the chemical quality of willow foliage. Plant Soil 2009, 323, 213–224. [Google Scholar] [CrossRef]
  8. Weih, M.; Nordh, N.E. Determinants of biomass production in hybrid willows and prediction of field performance from pot studies. Tree Physiol. 2005, 25, 1197–1206. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  9. Weih, M. Genetic and environmental variation in spring and autumn phenology of biomass willows (Salix spp.): Effects on shoot growth and nitrogen economy. Tree Physiol. 2009, 29, 1479–1490. [Google Scholar] [CrossRef] [PubMed]
  10. Robinson, K.M.; Karp, A.; Taylor, G. Defining leaf traits linked to yield in short-rotation coppice Salix. Biomass Bioenergy 2004, 26, 417–431. [Google Scholar] [CrossRef]
  11. Loreau, M.; Hector, A. Partitioning selection and complementarity in biodiversity experiments. Nature 2001, 412, 72–76. [Google Scholar] [CrossRef] [PubMed]
  12. Tilman, D.; Isbell, F.; Cowles, J.M. Biodiversity and Ecosystem Functioning. In Annual Review of Ecology, Evolution, and Systematics, Volume 45; Futuyma, D.J., Ed.; Annual Reviews: Palo Alto, CA, USA, 2014; Volume 45, pp. 471–493. [Google Scholar]
  13. Schulze, E.D.; Bouriaud, O.; Weber, U.; Roscher, C.; Hessenmoeller, D.; Kroiher, F.; Schall, P. Management breaks the natural productivity-biodiversity relationship in forests and grassland: An opinion. For. Ecosyst. 2018, 5. [Google Scholar] [CrossRef]
  14. O’Connor, M.I.; Gonzalez, A.; Byrnes, J.E.K.; Cardinale, B.J.; Duffy, J.E.; Gamfeldt, L.; Griffin, J.N.; Hooper, D.; Hungate, B.A.; Paquette, A.; et al. A general biodiversity-function relationship is mediated by trophic level. Oikos 2017, 126, 18–31. [Google Scholar] [CrossRef]
  15. Holzwarth, F.; Ruger, N.; Wirth, C. Taking a closer look: Disentangling effects of functional diversity on ecosystem functions with a trait-based model across hierarchy and time. R. Soc. Open Sci. 2015, 2, 19. [Google Scholar] [CrossRef] [PubMed]
  16. Weih, M.; Ronnberg-Wastljung, A.; Glynn, C. Genetic basis of phenotypic correlations among growth traits in hybrid willow (Salix dasyclados x S-viminalis) grown under two water regimes. New Phytol. 2006, 170, 467–477. [Google Scholar] [CrossRef] [PubMed]
  17. Weih, M.; Bonosi, L.; Ghelardini, L.; Ronnberg-Wastljung, A.C. Optimizing nitrogen economy under drought: Increased leaf nitrogen is an acclimation to water stress in willow (Salix spp.). Ann. Bot. 2011, 108, 1347–1353. [Google Scholar] [CrossRef] [PubMed]
  18. Agren, G.I.; Weih, M. Plant stoichiometry at different scales: Element concentration patterns reflect environment more than genotype. New Phytol. 2012, 194, 944–952. [Google Scholar] [CrossRef] [PubMed]
  19. Fransson, P.M.A.; Toljander, Y.K.; Baum, C.; Weih, M. Host plant-ectomycorrhizal fungus combination drives resource allocation in willow: Evidence for complex species interaction from a simple experiment. Ecoscience 2013, 20, 112–121. [Google Scholar] [CrossRef]
  20. Puentes, A.; Torp, M.; Weih, M.; Bjorkman, C. Direct effects of elevated temperature on a tri-trophic system: Salix, leaf beetles and predatory bugs. Arthropod Plant Interact. 2015, 9, 567–575. [Google Scholar] [CrossRef]
  21. Hoeber, S.; Arranz, C.; Nordh, N.E.; Baum, C.; Low, M.; Nock, C.; Scherer-Lorenzen, M.; Weih, M. Genotype identity has a more important influence than genotype diversity on shoot biomass productivity in willow short-rotation coppices. Glob. Chang. Biol. Bioenergy 2018, 10, 534–547. [Google Scholar] [CrossRef]
  22. Schuldt, A.; Assmann, T.; Brezzi, M.; Buscot, F.; Eichenberg, D.; Gutknecht, J.; Hardtle, W.; He, J.S.; Klein, A.M.; Kuhn, P.; et al. Biodiversity across trophic levels drives multifunctionality in highly diverse forests. Nat. Commun. 2018, 9, 10. [Google Scholar] [CrossRef]
  23. Weih, M.; Hoeber, S.; Beyer, F.; Fransson, P. Traits to ecosystems: The ecological sustainability challenge when developing future energy crops. Front. Energy Res. 2014, 2, 1–5. [Google Scholar] [CrossRef]
  24. Albertsson, J.; Verwijst, T.; Hansson, D.; Bertholdsson, N.O.; Ahman, I. Effects of competition between short-rotation willow and weeds on performance of different clones and associated weed flora during the first harvest cycle. Biomass Bioenergy 2014, 70, 364–372. [Google Scholar] [CrossRef]
  25. Welc, M.; Lundkvist, A.; Verwijst, T. Effects of Cutting Phenology (Non-dormant Versus Dormant) on Early Growth Performance of Three Willow Clones Grown Under Different Weed Treatments and Planting Dates. Bioenergy Res. 2017, 10, 1094–1104. [Google Scholar] [CrossRef] [Green Version]
  26. Baum, S.; Weih, M.; Busch, G.; Kroiher, F.; Bolte, A. The impact of Short Rotation Coppice plantations on phytodiversity. Landbauforsch. Volkenrode 2009, 59, 163–170. [Google Scholar]
  27. Baum, S.; Bolte, A.; Weih, M. High value of short rotation coppice plantations for phytodiversity in rural landscapes. Glob. Chang. Biol. Bioenergy 2012, 4, 728–738. [Google Scholar] [CrossRef]
  28. Odum, E.P. Srategy of ecosystem development. Science 1969, 164, 262. [Google Scholar] [CrossRef] [PubMed]
  29. Schneider, E.D.; Kay, J.J. Life as a manifestation of the 2nd law of thermodynamics. Math. Comput. Model. 1994, 19, 25–48. [Google Scholar] [CrossRef]
  30. Isbell, F.; Calcagno, V.; Hector, A.; Connolly, J.; Harpole, W.S.; Reich, P.B.; Scherer-Lorenzen, M.; Schmid, B.; Tilman, D.; van Ruijven, J.; et al. High plant diversity is needed to maintain ecosystem services. Nature 2011, 477, 199–202. [Google Scholar] [CrossRef]
  31. Liang, J.J.; Crowther, T.W.; Picard, N.; Wiser, S.; Zhou, M.; Alberti, G.; Schulze, E.D.; McGuire, A.D.; Bozzato, F.; Pretzsch, H.; et al. Positive biodiversity-productivity relationship predominant in global forests. Science 2016, 354, 12. [Google Scholar] [CrossRef]
  32. Verheyen, K.; Vanhellemont, M.; Auge, H.; Baeten, L.; Baraloto, C.; Barsoum, N.; Bilodeau-Gauthier, S.; Bruelheide, H.; Castagneyrol, B.; Godbold, D.; et al. Contributions of a global network of tree diversity experiments to sustainable forest plantations. AMBIO 2016, 45, 29–41. [Google Scholar] [CrossRef]
  33. Tilman, D.; Lehman, C.L.; Thomson, K.T. Plant diversity and ecosystem productivity: Theoretical considerations. Proc. Natl. Acad. Sci. USA 1997, 94, 1857–1861. [Google Scholar] [CrossRef] [Green Version]
  34. Turnbull, L.A.; Levine, J.M.; Loreau, M.; Hector, A. Coexistence, niches and biodiversity effects on ecosystem functioning. Ecol. Lett. 2013, 16, 116–127. [Google Scholar] [CrossRef]
  35. Grossman, J.J.; Vanhellemont, M.; Barsoum, N.; Bauhus, J.; Bruelheide, H.; Castagneyrol, B.; Cavender-Bares, J.; Eisenhauer, N.; Ferlian, O.; Gravel, D.; et al. Synthesis and future research directions linking tree diversity to growth, survival, and damage in a global network of tree diversity experiments. Environ. Exp. Bot. 2018, 152, 68–89. [Google Scholar] [CrossRef]
  36. Hoeber, S.; Fransson, P.; Prieto-Ruiz, I.; Manzoni, S.; Weih, M. Two Salix Genotypes Differ in Productivity and Nitrogen Economy When Grown in Monoculture and Mixture. Front. Plant Sci. 2017, 8, 12. [Google Scholar] [CrossRef]
  37. Dillen, M.; Vanhellemont, M.; Verdonckt, P.; Maes, W.H.; Steppe, K.; Verheyen, K. Productivity, stand dynamics and the selection effect in a mixed willow clone short rotation coppice plantation. Biomass Bioenergy 2016, 87, 46–54. [Google Scholar] [CrossRef]
  38. Mundt, C.C. Use of multiline cultivars and cultivar mixtures for disease management. Annu. Rev. Phytopathol. 2002, 40, 381–410. [Google Scholar] [CrossRef]
  39. Dawson, W.M.; McCracken, A.R. The performance of polyclonal stands in short rotation coppice willow for energy production. Biomass Bioenergy 1995, 8, 1–5. [Google Scholar] [CrossRef]
  40. McCracken, A.R.; Walsh, L.; Moore, P.J.; Lynch, M.; Cowan, P.; Dawson, M.; Watson, S. Yield of willow (Salix spp.) grown in short rotation coppice mixtures in a long-term trial. Ann. Appl. Biol. 2011, 159, 229–243. [Google Scholar] [CrossRef]
  41. Castagneyrol, B.; Jactel, H.; Vacher, C.; Brockerhoff, E.G.; Koricheva, J. Effects of plant phylogenetic diversity on herbivory depend on herbivore specialization. J. Appl. Ecol. 2014, 51, 134–141. [Google Scholar] [CrossRef]
  42. McCracken, A.R.; Dawson, W.M. Growing clonal mixtures of willow to reduce effect of Melampsora epitea var. epitea. Eur. J. For. Pathol. 1997, 27, 319–329. [Google Scholar] [CrossRef]
  43. Plath, M.; Dorn, S.; Riedel, J.; Barrios, H.; Mody, K. Associational resistance and associational susceptibility: Specialist herbivores show contrasting responses to tree stand diversification. Oecologia 2012, 169, 477–487. [Google Scholar] [CrossRef]
  44. Schuldt, A.; Bruelheide, H.; Hardtle, W.; Assmann, T.; Li, Y.; Ma, K.P.; von Oheimb, G.; Zhang, J.Y. Early positive effects of tree species richness on herbivory in a large-scale forest biodiversity experiment influence tree growth. J. Ecol. 2015, 103, 563–571. [Google Scholar] [CrossRef]
  45. Cardinale, B.J.; Duffy, J.E.; Gonzalez, A.; Hooper, D.U.; Perrings, C.; Venail, P.; Narwani, A.; Mace, G.M.; Tilman, D.; Wardle, D.A.; et al. Biodiversity loss and its impact on humanity. Nature 2012, 486, 59–67. [Google Scholar] [CrossRef]
  46. Whitham, T.G.; Bailey, J.K.; Schweitzer, J.A.; Shuster, S.M.; Bangert, R.K.; LeRoy, C.J.; Lonsdorf, E.V.; Allan, G.J.; DiFazio, S.P.; Potts, B.M.; et al. A framework for community and ecosystem genetics: From genes to ecosystems. Nat. Rev. Genet. 2006, 7, 510–523. [Google Scholar] [CrossRef]
  47. Koricheva, J.; Hayes, D. The relative importance of plant intraspecific diversity in structuring arthropod communities: A meta-analysis. Funct. Ecol. 2018, 32, 1704–1717. [Google Scholar] [CrossRef]
  48. Fritz, R.S.; Price, P.W. Genetic variation among plants and insect community structure—Willows and sawflies. Ecology 1988, 69, 845–856. [Google Scholar] [CrossRef]
  49. Fritz, R.S. Direct and indirect effects of plant genetic variation on enemy impact. Ecol. Entomol. 1995, 20, 18–26. [Google Scholar] [CrossRef]
  50. Larsson, S.; Strong, D.R. Oviposition choice and larval survival of Dasineura marginemtorquens (Diptera, Cecidomyiidae) on resistant and susceptible Salix viminalis. Ecol. Entomol. 1992, 17, 227–232. [Google Scholar] [CrossRef]
  51. Hochwender, C.G.; Fritz, R.S. Plant genetic differences influence herbivore community structure: Evidence from a hybrid willow system. Oecologia 2004, 138, 547–557. [Google Scholar] [CrossRef]
  52. Dalin, P.; Kindvall, O.; Bjorkman, C. Reduced Population Control of an Insect Pest in Managed Willow Monocultures. PLoS ONE 2009, 4. [Google Scholar] [CrossRef]
  53. Glynn, C.; Larsson, S. Rapid gall midge adaptation to a resistant willow genotype. Agric. For. Entomol. 2000, 2, 115–121. [Google Scholar] [CrossRef]
  54. Glynn, C.; Herms, D.A.; Orians, C.M.; Hansen, R.C.; Larsson, S. Testing the growth-differentiation balance hypothesis: Dynamic responses of willows to nutrient availability. New Phytol. 2007, 176, 623–634. [Google Scholar] [CrossRef]
  55. Muller, M.; Klein, A.M.; Scherer-Lorenzen, M.; Nock, C.A.; Staab, M. Tree genetic diversity increases arthropod diversity in willow short rotation coppice. Biomass Bioenergy 2018, 108, 338–344. [Google Scholar] [CrossRef]
  56. Moritz, K.K.; Parachnowitsch, A.L.; Julkunen-Tiitto, R.; Bjorkman, C.; Ayres, M.P.; Stenberg, J.A. Roe deer prefer mixed-sex willow stands over monosexual stands but do not discriminate between male and female plants. Environ. Exp. Bot. 2018, 146, 62–67. [Google Scholar] [CrossRef]
  57. Kaplan, I.; Thaler, J.S. Do plant defenses enhance or diminish prey suppression by omnivorous Heteroptera? Biol. Control 2011, 59, 53–60. [Google Scholar] [CrossRef]
  58. Bjorkman, C.; Hoglund, S.; Eklund, K.; Larsson, S. Effects of leaf beetle damage on stem wood production in coppicing willow. Agric. For. Entomol. 2000, 2, 131–139. [Google Scholar] [CrossRef]
  59. Moreira, X.; Abdala-Roberts, L.; Rasmann, S.; Castagneyrol, B.; Mooney, K.A. Plant diversity effects on insect herbivores and their natural enemies: Current thinking, recent findings, and future directions. Curr. Opin. Insect Sci. 2016, 14, 1–7. [Google Scholar] [CrossRef]
  60. Ronnberg-Wastljung, A.C.; Ahman, I.; Glynn, C.; Widenfalk, O. Quantitative trait loci for resistance to herbivores in willow: Field experiments with varying soils and climates. Entomol. Exp. Appl. 2006, 118, 163–174. [Google Scholar] [CrossRef]
  61. Smith, S.E.; Read, D.J. Mycorrhizal Symbiosis, 3rd ed.; Academic Press: Cambridge, MA, USA, 2008. [Google Scholar]
  62. Vander Heijden, E.W. Differential benefits of arbuscular mycorrhizal and ectomycorrhizal infection of Salix repens. Mycorrhiza 2001, 10, 185–193. [Google Scholar] [CrossRef]
  63. Simard, S.W.; Durall, D.M. Mycorrhizal networks: A review of their extent, function, and importance. Can. J. Bot. Rev. Can. Bot. 2004, 82, 1140–1165. [Google Scholar] [CrossRef]
  64. Rooney, D.C.; Killham, K.; Bending, G.D.; Baggs, E.; Weih, M.; Hodge, A. Mycorrhizas and biomass crops: Opportunities for future sustainable development. Trends Plant Sci. 2009, 14, 542–549. [Google Scholar] [CrossRef]
  65. Baum, C.; Leinweber, P.; Weih, M.; Lamersdorf, N.; Dimitriou, I. Effects of short rotation coppice with willows and poplar on soil ecology. Landbauforsch. Volkenrode 2009, 59, 183–196. [Google Scholar]
  66. Lange, M.; Eisenhauer, N.; Sierra, C.A.; Bessler, H.; Engels, C.; Griffiths, R.I.; Mellado-Vazquez, P.G.; Malik, A.A.; Roy, J.; Scheu, S.; et al. Plant diversity increases soil microbial activity and soil carbon storage. Nat. Commun. 2015, 6, 8. [Google Scholar] [CrossRef]
  67. Gamfeldt, L.; Snall, T.; Bagchi, R.; Jonsson, M.; Gustafsson, L.; Kjellander, P.; Ruiz-Jaen, M.C.; Froberg, M.; Stendahl, J.; Philipson, C.D.; et al. Higher levels of multiple ecosystem services are found in forests with more tree species. Nat. Commun. 2013, 4, 8. [Google Scholar] [CrossRef]
  68. Simard, S.W.; Jones, M.D.; Durall, D.M. Carbon and nutrient fluxes within and between mycorrhizal plants. Mycorrhizal Ecol. 2002, 157, 33–74. [Google Scholar]
  69. Clemmensen, K.E.; Bahr, A.; Ovaskainen, O.; Dahlberg, A.; Ekblad, A.; Wallander, H.; Stenlid, J.; Finlay, R.D.; Wardle, D.A.; Lindahl, B.D. Roots and Associated Fungi Drive Long-Term Carbon Sequestration in Boreal Forest. Science 2013, 339, 1615–1618. [Google Scholar] [CrossRef]
  70. Schimel, J.P.; Schaeffer, S.M. Microbial control over carbon cycling in soil. Front. Microbiol. 2012, 3, 11. [Google Scholar] [CrossRef]
  71. Agerer, R. Exploration types of ectomycorrhizae—A proposal to classify ectomycorrhizal mycelial systems according to their patterns of differentiation and putative ecological importance. Mycorrhiza 2001, 11, 107–114. [Google Scholar] [CrossRef]
  72. Soudzilovskaia, N.A.; van der Heijden, M.G.A.; Cornelissen, J.H.C.; Makarov, M.I.; Onipchenko, V.G.; Maslov, M.N.; Akhmetzhanova, A.A.; van Bodegom, P.M. Quantitative assessment of the differential impacts of arbuscular and ectomycorrhiza on soil carbon cycling. New Phytol. 2015, 208, 280–293. [Google Scholar] [CrossRef]
  73. Baum, C.; Eckhardt, K.U.; Hahn, J.; Weih, M.; Dimitriou, I.; Leinweber, P. Impact of poplar on soil organic matter quality and microbial communities in arable soils. Plant Soil Environ. 2013, 59, 95–100. [Google Scholar] [CrossRef]
  74. Baum, C.; Hrynkiewicz, K.; Leinweber, P.; Meissner, R. Heavy-metal mobilization and uptake by mycorrhizal and nonmycorrhizal willows (Salix x dasyclados). J. Plant Nutr. Soil Sci. Z. Pflanzenernahr. Bodenkd. 2006, 169, 516–522. [Google Scholar] [CrossRef]
  75. Fillion, M.; Brisson, J.; Guidi, W.; Labrecque, M. Increasing phosphorus removal in willow and poplar vegetation filters using arbuscular mycorrhizal fungi. Ecol. Eng. 2011, 37, 199–205. [Google Scholar] [CrossRef]
  76. Baum, C.; Hrynkiewicz, K. Clonal and seasonal shifts in communities of saprotrophic microfungi and soil enzyme activities in the mycorrhizosphere of Salix spp. J. Plant Nutr. Soil Sci. Z. Pflanzenernahr. Bodenkd. 2006, 169, 481–487. [Google Scholar] [CrossRef]
  77. Hrynkiewicz, K.; Baum, C.; Leinweber, P.; Weih, M.; Dimitriou, I. The significance of rotation periods for mycorrhiza formation in Short Rotation Coppice. For. Ecol. Manag. 2010, 260, 1943–1949. [Google Scholar] [CrossRef]
  78. Hrynkiewicz, K.; Toljander, Y.K.; Baum, C.; Fransson, P.M.A.; Taylor, A.F.S.; Weih, M. Correspondence of ectomycorrhizal diversity and colonisation of willows (Salix spp.) grown in short rotation coppice on arable sites and adjacent natural stands. Mycorrhiza 2012, 22, 603–613. [Google Scholar] [CrossRef]
  79. Vanbeveren, S.P.P.; Ceulemans, R. Biodiversity in short-rotation coppice. Renew. Sustain. Energy Rev. 2019, 111, 34–43. [Google Scholar] [CrossRef]
  80. Baum, C.; Hrynkiewicz, K.; Szymanska, S.; Vitow, N.; Hoeber, S.; Fransson, P.M.A.; Weih, M. Mixture of Salix Genotypes Promotes Root Colonization with Dark Septate Endophytes and Changes P Cycling in the Mycorrhizosphere. Front. Microbiol. 2018, 9, 10. [Google Scholar] [CrossRef]
  81. Crotty, F.V.; Blackshaw, R.P.; Adl, S.M.; Inger, R.; Murray, P.J. Divergence of feeding channels within the soil food web determined by ecosystem type. Ecol. Evol. 2014, 4, 1–13. [Google Scholar] [CrossRef]
  82. Bakker, M.R.; Brunner, I.; Ashwood, F.; Bjarnadottir, B.; Bolger, T.; Børja, I.; Carnol, M.; Cudlin, P.; Dalsgaard, L.; Erktan, A.; et al. Belowground Biodiversity Relates Positively to Ecosystem Services of European Forests. Front. For. Glob. Chang. 2019, 2. [Google Scholar] [CrossRef] [Green Version]
  83. Kuzovkina, Y.A.; Weih, M.; Abalos Romero, M.; Charles, J.; Hurst, S.; McIvor, I.; Karp, A.; Trybush, S.; Labrecque, M.; Teodorescu, T.I. Salix: Botany and global horticulture. Hortic. Rev. 2008, 34, 447–489. [Google Scholar]
  84. Fabio, E.S.; Smart, L.B. Differential growth response to fertilization of ten elite shrub willow (Salix spp.) bioenergy cultivars. Trees Struct. Funct. 2018, 32, 1061–1072. [Google Scholar] [CrossRef]
  85. Connolly, J.; Cadotte, M.W.; Brophy, C.; Dooley, A.; Finn, J.; Kirwan, L.; Roscher, C.; Weigelt, A. Phylogenetically diverse grasslands are associated with pairwise interspecific processes that increase biomass. Ecology 2011, 92, 1385–1392. [Google Scholar] [CrossRef]
  86. Bell, T.; Newman, J.A.; Silverman, B.W.; Turner, S.L.; Lilley, A.K. The contribution of species richness and composition to bacterial services. Nature 2005, 436, 1157–1160. [Google Scholar] [CrossRef]
  87. Bell, T.; Lilley, A.K.; Hector, A.; Schmid, B.; King, L.; Newman, J.A. A Linear Model Method for Biodiversity-Ecosystem Functioning Experiments. Am. Nat. 2009, 174, 836–849. [Google Scholar] [CrossRef]
  88. Connolly, J.; Bell, T.; Bolger, T.; Brophy, C.; Carnus, T.; Finn, J.A.; Kirwan, L.; Isbell, F.; Levine, J.; Luescher, A.; et al. An improved model to predict the effects of changing biodiversity levels on ecosystem function. J. Ecol. 2013, 101, 344–355. [Google Scholar] [CrossRef] [Green Version]
  89. Brophy, C.; Dooley, A.; Kirwan, L.; Finn, J.A.; McDonnell, J.; Bell, T.; Cadotte, M.W.; Connolly, J. Biodiversity and ecosystem function: Making sense of numerous species interactions in multi-species communities. Ecology 2017, 98, 1771–1778. [Google Scholar] [CrossRef]
Diversity 11 00125 g001 550
Figure 1. Conceptual overview of important relationships between plant (willow) traits and the biodiversity–ecosystem function (BEF) components and processes to be targeted when developing predictive BEF theory using willow short-rotation coppice (SRC) as a model. The BEF components relate to plant growth and productivity (green), insect herbivory as an important above ground trophic interaction (red), and soil microbes representing an important part of below ground trophic interactions (yellow). The BEF processes listed are considered important for the functioning of plant communities. Modified from [23].
Figure 1. Conceptual overview of important relationships between plant (willow) traits and the biodiversity–ecosystem function (BEF) components and processes to be targeted when developing predictive BEF theory using willow short-rotation coppice (SRC) as a model. The BEF components relate to plant growth and productivity (green), insect herbivory as an important above ground trophic interaction (red), and soil microbes representing an important part of below ground trophic interactions (yellow). The BEF processes listed are considered important for the functioning of plant communities. Modified from [23].
Diversity 11 00125 g001
Diversity 11 00125 g002 550
Figure 2. Overview of the links between ecosystem characteristics and processes currently researched in willow SRC systems (thin arrows), separated into bottom-up (solid lines) and top-down (dashed lines) interactions; and their connections to the overall ecosystem processes important for biodiversity–ecosystem function (BEF) (thick arrows). Bottom-up processes are those in which plant growth is affected by the utilization of limited resources (e.g., nutrient elements), while top-down processes are those in which plant growth is affected by the action of predators feeding on herbivores. Photo: Mixed willow SRC plantation near Uppsala, Sweden; the willow shoots are three years old (courtesy S. Hoeber, SLU).
Figure 2. Overview of the links between ecosystem characteristics and processes currently researched in willow SRC systems (thin arrows), separated into bottom-up (solid lines) and top-down (dashed lines) interactions; and their connections to the overall ecosystem processes important for biodiversity–ecosystem function (BEF) (thick arrows). Bottom-up processes are those in which plant growth is affected by the utilization of limited resources (e.g., nutrient elements), while top-down processes are those in which plant growth is affected by the action of predators feeding on herbivores. Photo: Mixed willow SRC plantation near Uppsala, Sweden; the willow shoots are three years old (courtesy S. Hoeber, SLU).
Diversity 11 00125 g002
Table
Table 1. Ranges of functional trait values observed in similar-aged willow genotypes field-grown in SRC systems in Sweden and UK; the smallest (Minimum) and highest (Maximum) values observed in any of the genotypes grown in the respective trial are shown.
Table 1. Ranges of functional trait values observed in similar-aged willow genotypes field-grown in SRC systems in Sweden and UK; the smallest (Minimum) and highest (Maximum) values observed in any of the genotypes grown in the respective trial are shown.
TraitMinimumMaximumGenotypes and Growth ConditionsSource
Shoot biomass per plant (kg)0.31.56 genotypes, 4 treatments[8]
Total leaf area (m2)0.62.5
Root biomass fraction (-)0.10.2
Specific leaf area (mm2 g−1)952413,089
Leaf N concentration (%)1.73.3
Bud burst date (day of year)761156 genotypes, 4 treatments[9]
Biomass yield (Mg ha−1 year−1)6165 genotypes, 1 treatment[10]
Specific leaf area (mm2 g−1)12,12914,923
Final individual leaf area (mm2)20604573

Share and Cite

MDPI and ACS Style

Weih, M.; Glynn, C.; Baum, C. Willow Short-Rotation Coppice as Model System for Exploring Ecological Theory on Biodiversity–Ecosystem Function. Diversity 2019, 11, 125. https://doi.org/10.3390/d11080125

AMA Style

Weih M, Glynn C, Baum C. Willow Short-Rotation Coppice as Model System for Exploring Ecological Theory on Biodiversity–Ecosystem Function. Diversity. 2019; 11(8):125. https://doi.org/10.3390/d11080125

Chicago/Turabian Style

Weih, Martin, Carolyn Glynn, and Christel Baum. 2019. "Willow Short-Rotation Coppice as Model System for Exploring Ecological Theory on Biodiversity–Ecosystem Function" Diversity 11, no. 8: 125. https://doi.org/10.3390/d11080125

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop