- Email: [email protected]
Forest Ecological Intensification
Technical advances will be helpful in addressing these questions. For example, single-molecular imaging is a powerful technique that can reveal dynamic protein interactions in living cells. Lightsheet fluorescence microscopy allows long-term and in-depth imaging at single-cell resolution that is particularly effective for studying plant cell development. In addition, the emergence of the proximity labeling-based spatial proteomics holds promise for resolving protein interaction Although recent discoveries have improved networks that underlie cell signaling our understanding of cell polarity in the reg- processes. ulation of stomatal ACD, several outstanding questions remain to be addressed. (i) What is the molecular mechanism Acknowledgments underlying protein polarization in Research by the group of J.D. is supported by the National Institute of General Medical Sciences of the the stomatal ACD system? MAPKNational Institutes of Health under award number and BIN2-mediated phosphorylation R01GM109080. may promote BASL/POLAR polarization [4,7], but the mechanisms 1Waksman Institute of Microbiology, Rutgers, The State University of New Jersey, Piscataway, NJ 08854, USA by which these peripheral membrane 2Department of Plant Biology, Rutgers, The State proteins are polarly targeted and University of New Jersey, Piscataway, NJ 08901, USA maintained at the cortical membrane *Correspondence: [email protected] (J. Dong). domain remain a major challenge. https://doi.org/10.1016/j.tplants.2019.03.007 (ii) How is the polarity complex differentially assembled at different stages of © 2019 Elsevier Ltd. All rights reserved. stomatal ACD? The mechanism underlying the dynamic assembly of BIN2/GSK3s and YODA/MPK3/6 References at the polarity site is unknown, and its 1. MacAlister, C.A. et al. (2007) Transcription factor control of asymmetric cell divisions that establish the stomatal lineelucidation would give unique age. Nature, 445, 537–540 insights into the mechanisms that 2. Lampard, G.R. et al. (2008) Arabidopsis stomatal initiation is controlled by MAPK-mediated regulation of the bHLH balance cell division and fate differSPEECHLESS. Science, 322, 1113–1116 entiation in plant stem cells. 3. Gudesblat, G.E. et al. (2012) SPEECHLESS integrates brassinosteroid and stomata signalling pathways. Nat. Cell (iii) Direct physical relationships among Biol. 14, 548–554 the polarity factors (BASL, POLAR, 4. Houbaert, A. et al. (2018) POLAR-guided signalling complex assembly and localization drive asymmetric cell diviYODA, and BIN2/GSKs) need to be sion. Nature, 563, 574–578 elucidated to construct the dynamic 5. Dong, J. et al. (2009) BASL controls asymmetric cell diviarchitecture of the polarity modules sion in Arabidopsis. Cell, 137, 1320–1330 at different stages. In particular, evi- 6. Pillitteri, L.J. et al. (2011) Molecular profiling of stomatal meristemoids reveals new component of asymmetric cell dence of physical linkage between division and commonalities among stem cell populations in Arabidopsis. Plant Cell, 23, 3260–3275 BASL and POLAR is still lacking. Moreover, although BIN2/GSK3s 7. Zhang, Y. et al. (2015) The BASL polarity protein controls a MAPK signaling feedback loop in asymmetric cell division. suppress POLAR protein stability, Dev. Cell, 33, 136–149 positive regulator(s), so far unidenti- 8. He, J.X. et al. (2002) The GSK3-like kinase BIN2 phosphorylates and destabilizes BZR1, a positive regulator of fied, are anticipated to promote the brassinosteroid signaling pathway in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 99, 10185–10190 polarity formation by BASL/POLAR.
analysis is necessary for better characterization of such multifunctional signaling molecules. For example, BIN2 can be a positive or negative regulator in the BRactivated phloem differentiation process, depending on the presence or absence of the peripheral membrane protein OCTOPUS (OPS), respectively [12]. Where and when these signaling molecules function might be crucial in elucidating how they regulate a specific pathway.
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9. Kim, T.W. et al. (2009) Brassinosteroid signal transduction from cell-surface receptor kinases to nuclear transcription factors. Nat. Cell Biol. 11, 1254–1260 10. Kim, T.W. et al. (2012) Brassinosteroid regulates stomatal development by GSK3-mediated inhibition of a MAPK pathway. Nature, 482, 419–422 11. Gudesblat, G.E. et al. (2012) Brassinosteroids tailor stomatal production to different environments. Trends Plant Sci. 17, 685–687 12. Anne, P. et al. (2015) OCTOPUS negatively regulates BIN2 to control phloem differentiation in Arabidopsis thaliana. Curr. Biol. 25, 2584–2590
Forum
Forest Ecological Intensification Daniel Montesinos1,2,* Ecological intensification aims to counter-balance the negative impacts of agriculture intensification by promoting management interventions that maximize ecosystem services. However, the application of these principles to forestry is still pending. It is time for forestry to benefit from actively researching and implementing management policies based on ecological intensification. Forests are chief providers of ecosystem services, including supporting, provisioning, regulating, and cultural services, but the quantity and quality of such services are highly dependent on biodiversity [1–3]. More than 50% of global forests experience significant exploitation for wood and other nonwood forest products. Specifically, high demand for wood and fiber has resulted in dedicated forest plantations, which constitute 7.3% of the forests worldwide [4]. Unfortunately, forest plantations present some of the lowest biodiversity and ecosystem services of all forests [2]. They are often dominated by monocultures of exotic species,
(A) Agriculture
agroecosystems, there is a recent trend towards promoting ‘ecological intensifiMixed crop cation’ [6]. Ecological intensification is defined by the Food and Agriculture Organization of the United Nations (FAO) as ‘a knowledge-intensive process that requires optimal management of nature’s ecological functions and biodiversity to improve agricultural system perCrop rotaon Fallow formance, efficiency and farmers’ livelihoods’i. This approach intends to harness the benefits of increasing eco(B) system services and biodiversity in a way that maximizes production, but minForestry Mixed plantaon imizes environmental impacts by decreasing, but not excluding, the use of synthetic fertilizers, pesticides, or energy [6]. Ecological intensification is a response to some of the most negative effects of agricultural intensification, and it is gaining popularity, due to its down-toRotaon Fallow earth results-based approach. Ecological intensification includes practices that are recognized as good practices in both agriculture and forestry, including conserFigure 1. Ecological Intensification in Agricul- vation tillage, crop rotation, and mixed ture and Forestry. Example of practices promoted cropping (Figure 1). However, ecological by ecological intensification in (A) agriculture, and their potential correspondence in (B) forestry. Clockwise, intensification has not yet been explicitly top to bottom: mixed cropping/plantation, fallow, and applied to forest systems. rotation. In the center, the presence of landscape heterogeneity is represented: (A) in the form of hedges or natural and seminatural patches; (B) in the form of not only natural and seminatural forest patches, but also orchards or even diversified crops, which can in turn act as a source of biodiversity to exploited forests, resulting in increased ecosystem services and resilience to disturbance.
significantly reducing their ability to provide ecosystem services and making them highly susceptible to disturbances, such as fire or outbreaks of pests [4,5]. The intensification of both agriculture and forestry exploitations can be challenging in similar ways, including shared problems associated with the oversimplification of large extensions of land, often dominated by monocultures. In
Traditional low-intensity forest management has supported high biodiversity levels for centuries, and the environmental and economic benefits of increasing forest biodiversity are significant [7]. Diversified forests are significantly more productive, and also resilient to global change and to catastrophic disturbances [8]. Higher levels of plant diversity have been associated with higher diversity and abundance of predators, such as birds, spiders, or small mammals, which feed on insects and prevent pest outbreaks [5,8]. Diversified forests also host more diversified groups of microbes and fungi, which are essential to fix nitrogen; hence, diversified forests need less input and increase their productivity significantly [8–10]. Other services might not result in direct economic revenues for land managers,
but can provide important benefits for the larger community in the form of wood for fuel, food from hunting, wild fruit and fungi collection, carbon sequestration, and increased water availability [9]. Forest ecological intensification will encompass promoting good forestry practices and increasing the biodiversity of forest plantations. However, this will require not only active political incentives, but also technical and scientific knowledge adapted to specific regional, and biological contexts. Unfortunately, such knowledge is scarce for some important forest plantations. For instance, the two most commonly planted forest species in the world are eucalyptus and pines. However, the diversity of species able to thrive in these plantations is often limited by the ability of pines and eucalyptus to release into the environment chemical substances capable of inhibiting the germination and growth of other species, a well-documented phenomenon known as ‘allelopathy’ [11,12]. The effects of allelopathy tend to be species specific, and some species are able to thrive despite the presence of such chemical compounds [11]. Relatively inexpensive trials could identify potential sets of local species capable of tolerating the allelopathic compounds released by some of the more abundant and challenging forest plantations, such as eucalyptus and pine stands. Research goals providing valuable ecological information to managers should aim to: (i) systematically evaluate the patterns of above and below-ground diversity and, when necessary, compare them with post-disturbance or post-fire biodiversity, paying special attention to changes in the abundance of invasive species, and its inter-relation with fire regimes and previous biodiversity occurrence; (ii) take into account the multiple types of biotic interaction, including mutualists and antagonist species critical for plant survival and reproduction; and (iii) evaluate the role of tree chemistry on
Trends in Plant Science, June 2019, Vol. 24, No. 6
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determining the potential assortment of Additionally, biodiversity-rich forests species able to thrive in each specific have better public acceptance and recreational value, improving the public perforest type. ception of forestry and contributing to a The diversity of forest types would more diversified rural activity and, thus, require that managers and politicians to the greater economic and social stapromote local research with approaches bility of rural populations [3]. adapted to each specific forest type in each geographical area, but the returns Acknowledgments for such relatively small investments Thanks to the Portuguese Fundação para a Ciência e should pay off significantly in terms of a Tecnologia – FCT for funding (IF-00066-2013; productivity, resiliency, and public appre- PTDC/BIA-PLA/0763/2014), and to Rubén Milla, Sílciation. There is a clear correlation via Castro, Rúben Heleno, and Sergio Timóteo for feedback. between forest biodiversity and productivity, because increases in understory Resources biodiversity result in reduced soil erosion i www.fao.org/agriculture/crops/thematic-sitemap/ and increased soil fertility [8,13]. Biodi- theme/biodiversity/ecological-intensification/en/ versity also stabilizes ecological systems 1 and provides greater resilience to climate Australian Tropical Herbarium, James Cook University, McGregor Road, Smithfield 4878, QLD, Australia change and to catastrophic disturban- 2Centre for Functional Ecology, Department of Life ces, including pest outbreaks or fire, Sciences, University of Coimbra, Calçada Martim de which have large costs in terms of Freitas, Coimbra 3000–456, Portugal reduced productivity [5,14]. Conse- *Correspondence: quently, efforts to adopt good forestry [email protected] (D. Montesinos). practices and to increase biodiversity in https://doi.org/10.1016/j.tplants.2019.03.009 forest plantations could significantly © 2019 Elsevier Ltd. All rights reserved. increase their economic and ecological value at a marginal economic cost [15], with potential large returns for investment References in the long term, which is necessary for 1. Balvanera, P. et al. (2006) Quantifying the evidence for biodiversity effects on ecosystem functioning and services. the quantification of economic and Ecol. Lett. 9, 1146–1156 environmental returns in forestry.
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2. van der Plas, F. et al. (2016) Biotic homogenization can decrease landscape-scale forest multifunctionality. Proc. Natl. Acad. Sci. 113, 3557–3562 3. Chao, L. et al. (2011) In Landscape Ecology in Forest Management and Conservation. Higher Education Press–Springer 4. FAO (2016) Global Forest Resources Assessment 2015: How Have the World’s Forests Changed? FAO 5. Dwyer, G. et al. (2004) The combined effects of pathogens and predators on insect outbreaks. Nature 430, 341–345 6. Bommarco, R. et al. (2013) Ecological intensification: harnessing ecosystem services for food security. Trends Ecol. Evol. 28, 230–238 7. Tscharntke, T. et al. (2005) Landscape perspectives on agricultural intensification and biodiversity - ecosystem service management. Ecol. Lett. 8, 857–874 8. Thompson, I. et al. (2009) Forest Resilience, Biodiversity, and Climate Change. A Synthesis of the Biodiversity/Resilience/Stability Relationship in Forest Ecosystems, Secretariat of the Convention on Biological Diversity 9. Pimentel, D. et al. (1992) Conserving biological diversity in agricultural/forestry systems. Bioscience 42, 354–362 10. Hiiesalu, I. et al. (2017) Plant species richness and productivity determine the diversity of soil fungal guilds in temperate coniferous forest and bog habitats. Mol. Ecol. 26, 4846–4858 11. Becerra, P.I. et al. (2018) Inhibitory effects of Eucalyptus globulus on understorey plant growth and species richness are greater in non-native regions. Glob. Ecol. Biogeogr. 27, 68–76 12. Ismail, A. et al. (2013) Comparative study of two coniferous species (Pinus pinaster Aiton and Cupressus sempervirens L. var. dupreziana [A. Camus] Silba) essential oils: chemical composition and biological activity. Chil. J. Agric. Res. 73, 259–266 13. Brockerhoff, E.G. et al. (2013) Role of eucalypt and other planted forests in biodiversity conservation and the provision of biodiversity-related ecosystem services. For. Ecol. Manage. 301, 43–50 14. Macdougall, A.S. et al. (2013) Diversity loss with persistent human disturbance increases vulnerability to ecosystem collapse. Nature 494, 86–89 15. Payn, T. et al. (2015) Changes in planted forests and future global implications. For. Ecol. Manage. 352, 57–67
analysis is necessary for better characterization of such multifunctional signaling molecules. For example, BIN2 can be a positive or negative regulator in the BRactivated phloem differentiation process, depending on the presence or absence of the peripheral membrane protein OCTOPUS (OPS), respectively [12]. Where and when these signaling molecules function might be crucial in elucidating how they regulate a specific pathway.
484
Trends in Plant Science, June 2019, Vol. 24, No. 6
9. Kim, T.W. et al. (2009) Brassinosteroid signal transduction from cell-surface receptor kinases to nuclear transcription factors. Nat. Cell Biol. 11, 1254–1260 10. Kim, T.W. et al. (2012) Brassinosteroid regulates stomatal development by GSK3-mediated inhibition of a MAPK pathway. Nature, 482, 419–422 11. Gudesblat, G.E. et al. (2012) Brassinosteroids tailor stomatal production to different environments. Trends Plant Sci. 17, 685–687 12. Anne, P. et al. (2015) OCTOPUS negatively regulates BIN2 to control phloem differentiation in Arabidopsis thaliana. Curr. Biol. 25, 2584–2590
Forum
Forest Ecological Intensification Daniel Montesinos1,2,* Ecological intensification aims to counter-balance the negative impacts of agriculture intensification by promoting management interventions that maximize ecosystem services. However, the application of these principles to forestry is still pending. It is time for forestry to benefit from actively researching and implementing management policies based on ecological intensification. Forests are chief providers of ecosystem services, including supporting, provisioning, regulating, and cultural services, but the quantity and quality of such services are highly dependent on biodiversity [1–3]. More than 50% of global forests experience significant exploitation for wood and other nonwood forest products. Specifically, high demand for wood and fiber has resulted in dedicated forest plantations, which constitute 7.3% of the forests worldwide [4]. Unfortunately, forest plantations present some of the lowest biodiversity and ecosystem services of all forests [2]. They are often dominated by monocultures of exotic species,
(A) Agriculture
agroecosystems, there is a recent trend towards promoting ‘ecological intensifiMixed crop cation’ [6]. Ecological intensification is defined by the Food and Agriculture Organization of the United Nations (FAO) as ‘a knowledge-intensive process that requires optimal management of nature’s ecological functions and biodiversity to improve agricultural system perCrop rotaon Fallow formance, efficiency and farmers’ livelihoods’i. This approach intends to harness the benefits of increasing eco(B) system services and biodiversity in a way that maximizes production, but minForestry Mixed plantaon imizes environmental impacts by decreasing, but not excluding, the use of synthetic fertilizers, pesticides, or energy [6]. Ecological intensification is a response to some of the most negative effects of agricultural intensification, and it is gaining popularity, due to its down-toRotaon Fallow earth results-based approach. Ecological intensification includes practices that are recognized as good practices in both agriculture and forestry, including conserFigure 1. Ecological Intensification in Agricul- vation tillage, crop rotation, and mixed ture and Forestry. Example of practices promoted cropping (Figure 1). However, ecological by ecological intensification in (A) agriculture, and their potential correspondence in (B) forestry. Clockwise, intensification has not yet been explicitly top to bottom: mixed cropping/plantation, fallow, and applied to forest systems. rotation. In the center, the presence of landscape heterogeneity is represented: (A) in the form of hedges or natural and seminatural patches; (B) in the form of not only natural and seminatural forest patches, but also orchards or even diversified crops, which can in turn act as a source of biodiversity to exploited forests, resulting in increased ecosystem services and resilience to disturbance.
significantly reducing their ability to provide ecosystem services and making them highly susceptible to disturbances, such as fire or outbreaks of pests [4,5]. The intensification of both agriculture and forestry exploitations can be challenging in similar ways, including shared problems associated with the oversimplification of large extensions of land, often dominated by monocultures. In
Traditional low-intensity forest management has supported high biodiversity levels for centuries, and the environmental and economic benefits of increasing forest biodiversity are significant [7]. Diversified forests are significantly more productive, and also resilient to global change and to catastrophic disturbances [8]. Higher levels of plant diversity have been associated with higher diversity and abundance of predators, such as birds, spiders, or small mammals, which feed on insects and prevent pest outbreaks [5,8]. Diversified forests also host more diversified groups of microbes and fungi, which are essential to fix nitrogen; hence, diversified forests need less input and increase their productivity significantly [8–10]. Other services might not result in direct economic revenues for land managers,
but can provide important benefits for the larger community in the form of wood for fuel, food from hunting, wild fruit and fungi collection, carbon sequestration, and increased water availability [9]. Forest ecological intensification will encompass promoting good forestry practices and increasing the biodiversity of forest plantations. However, this will require not only active political incentives, but also technical and scientific knowledge adapted to specific regional, and biological contexts. Unfortunately, such knowledge is scarce for some important forest plantations. For instance, the two most commonly planted forest species in the world are eucalyptus and pines. However, the diversity of species able to thrive in these plantations is often limited by the ability of pines and eucalyptus to release into the environment chemical substances capable of inhibiting the germination and growth of other species, a well-documented phenomenon known as ‘allelopathy’ [11,12]. The effects of allelopathy tend to be species specific, and some species are able to thrive despite the presence of such chemical compounds [11]. Relatively inexpensive trials could identify potential sets of local species capable of tolerating the allelopathic compounds released by some of the more abundant and challenging forest plantations, such as eucalyptus and pine stands. Research goals providing valuable ecological information to managers should aim to: (i) systematically evaluate the patterns of above and below-ground diversity and, when necessary, compare them with post-disturbance or post-fire biodiversity, paying special attention to changes in the abundance of invasive species, and its inter-relation with fire regimes and previous biodiversity occurrence; (ii) take into account the multiple types of biotic interaction, including mutualists and antagonist species critical for plant survival and reproduction; and (iii) evaluate the role of tree chemistry on
Trends in Plant Science, June 2019, Vol. 24, No. 6
485
determining the potential assortment of Additionally, biodiversity-rich forests species able to thrive in each specific have better public acceptance and recreational value, improving the public perforest type. ception of forestry and contributing to a The diversity of forest types would more diversified rural activity and, thus, require that managers and politicians to the greater economic and social stapromote local research with approaches bility of rural populations [3]. adapted to each specific forest type in each geographical area, but the returns Acknowledgments for such relatively small investments Thanks to the Portuguese Fundação para a Ciência e should pay off significantly in terms of a Tecnologia – FCT for funding (IF-00066-2013; productivity, resiliency, and public appre- PTDC/BIA-PLA/0763/2014), and to Rubén Milla, Sílciation. There is a clear correlation via Castro, Rúben Heleno, and Sergio Timóteo for feedback. between forest biodiversity and productivity, because increases in understory Resources biodiversity result in reduced soil erosion i www.fao.org/agriculture/crops/thematic-sitemap/ and increased soil fertility [8,13]. Biodi- theme/biodiversity/ecological-intensification/en/ versity also stabilizes ecological systems 1 and provides greater resilience to climate Australian Tropical Herbarium, James Cook University, McGregor Road, Smithfield 4878, QLD, Australia change and to catastrophic disturban- 2Centre for Functional Ecology, Department of Life ces, including pest outbreaks or fire, Sciences, University of Coimbra, Calçada Martim de which have large costs in terms of Freitas, Coimbra 3000–456, Portugal reduced productivity [5,14]. Conse- *Correspondence: quently, efforts to adopt good forestry [email protected] (D. Montesinos). practices and to increase biodiversity in https://doi.org/10.1016/j.tplants.2019.03.009 forest plantations could significantly © 2019 Elsevier Ltd. All rights reserved. increase their economic and ecological value at a marginal economic cost [15], with potential large returns for investment References in the long term, which is necessary for 1. Balvanera, P. et al. (2006) Quantifying the evidence for biodiversity effects on ecosystem functioning and services. the quantification of economic and Ecol. Lett. 9, 1146–1156 environmental returns in forestry.
486
Trends in Plant Science, June 2019, Vol. 24, No. 6
2. van der Plas, F. et al. (2016) Biotic homogenization can decrease landscape-scale forest multifunctionality. Proc. Natl. Acad. Sci. 113, 3557–3562 3. Chao, L. et al. (2011) In Landscape Ecology in Forest Management and Conservation. Higher Education Press–Springer 4. FAO (2016) Global Forest Resources Assessment 2015: How Have the World’s Forests Changed? FAO 5. Dwyer, G. et al. (2004) The combined effects of pathogens and predators on insect outbreaks. Nature 430, 341–345 6. Bommarco, R. et al. (2013) Ecological intensification: harnessing ecosystem services for food security. Trends Ecol. Evol. 28, 230–238 7. Tscharntke, T. et al. (2005) Landscape perspectives on agricultural intensification and biodiversity - ecosystem service management. Ecol. Lett. 8, 857–874 8. Thompson, I. et al. (2009) Forest Resilience, Biodiversity, and Climate Change. A Synthesis of the Biodiversity/Resilience/Stability Relationship in Forest Ecosystems, Secretariat of the Convention on Biological Diversity 9. Pimentel, D. et al. (1992) Conserving biological diversity in agricultural/forestry systems. Bioscience 42, 354–362 10. Hiiesalu, I. et al. (2017) Plant species richness and productivity determine the diversity of soil fungal guilds in temperate coniferous forest and bog habitats. Mol. Ecol. 26, 4846–4858 11. Becerra, P.I. et al. (2018) Inhibitory effects of Eucalyptus globulus on understorey plant growth and species richness are greater in non-native regions. Glob. Ecol. Biogeogr. 27, 68–76 12. Ismail, A. et al. (2013) Comparative study of two coniferous species (Pinus pinaster Aiton and Cupressus sempervirens L. var. dupreziana [A. Camus] Silba) essential oils: chemical composition and biological activity. Chil. J. Agric. Res. 73, 259–266 13. Brockerhoff, E.G. et al. (2013) Role of eucalypt and other planted forests in biodiversity conservation and the provision of biodiversity-related ecosystem services. For. Ecol. Manage. 301, 43–50 14. Macdougall, A.S. et al. (2013) Diversity loss with persistent human disturbance increases vulnerability to ecosystem collapse. Nature 494, 86–89 15. Payn, T. et al. (2015) Changes in planted forests and future global implications. For. Ecol. Manage. 352, 57–67