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PERSPECTIVE article

Front. Sustain. Food Syst., 28 March 2022
Sec. Waste Management in Agroecosystems
This article is part of the Research Topic Upcycling Organic Waste for the Sustainable Management of Soilborne Pests and Pathogens in Agri-Food Systems View all 15 articles

Integrated Soil Health Management for Plant Health and One Health: Lessons From Histories of Soil-borne Disease Management in California Strawberries and Arthropod Pest Management

\nJoji Muramoto,,
Joji Muramoto1,2,3*Damian Michael Parr,Damian Michael Parr2,3Jan PerezJan Perez2Darryl G. Wong,Darryl G. Wong2,3
  • 1Division of Agriculture and Natural Resources, University of California, Santa Cruz, Santa Cruz, CA, United States
  • 2Center for Agroecology, University of California, Santa Cruz, Santa Cruz, CA, United States
  • 3Department of Environmental Studies, University of California, Santa Cruz, Santa Cruz, CA, United States

Many soil health assessment methods are being developed. However, they often lack assessment of soil-borne diseases. To better address management strategies for soil-borne disease and overall soil and plant health, the concept of Integrated Soil Health Management (ISHM) is explored. Applying the concept of Integrated Pest Management and an agroecological transdisciplinary approach, ISHM offers a framework under which a structure for developing and implementing biointensive soil health management strategies for a particular agroecosystem is defined. As a case study, a history of soil-borne disease management in California strawberries is reviewed and contrasted with a history of arthropod pest management to illustrate challenges associated with soil-borne disease management and the future directions of soil health research and soil-borne disease management. ISHM system consists of comprehensive soil health diagnostics, farmers' location-specific knowledge and adaptability, a suite of soil health management practices, and decision support tools. As we better understand plant-soil-microorganism interactions, including the mechanisms of soil suppressiveness, a range of diagnostic methodologies and indicators and their action thresholds may be developed. These knowledge-intensive and location-specific management systems require transdisciplinary approaches and social learning to be co-developed with stakeholders. The ISHM framework supports research into the broader implications of soil health such as the “One health” concept, which connects soil health to the health of plants, animals, humans, and ecosystems and research on microbiome and nutrient cycling that may better explain these interdependencies.

Introduction

The concept of soil health recognizes soil as a living ecosystem with one of the greatest diversities on the earth. These organisms interact with each other, plants, and the complex abiotic environment (Wall et al., 2012; Orgiazzi et al., 2016; USDA-NRCS, 2021). Healthy soil can provide multiple ecosystem services such as food and fiber production, water quality and supply, pest and disease suppression, atmospheric composition, and climate regulation, and biodiversity conservation (Kibblewhite et al., 2008; Lehman et al., 2015; Bünemann et al., 2018).

Many laboratory-based soil health assessment methods and indicators have also been proposed and developed (Andrews et al., 2004; Moebius-Clune et al., 2016; Stott, 2019; Norris et al., 2020). These typically analyze chemical (pH, electrical conductivity, available nutrients contents, soil organic carbon, labile carbon, potentially mineralizable nitrogen, protein nitrogen, etc.), physical (water-stable aggregates, slake test, bulk density, etc.), and biological (various enzyme activities, respiration, microbial biomass, phospholipid fatty acid, etc.) properties. Yet, they often lack the assessment of soil-borne diseases. According to the Web of Science database, 3,120 papers were published on the topic “soil health” between 2000 and 2020. Among these, only 4.7% included topics of “soil-borne (or soilborne) pathogen,” “soil-borne (or soilborne) disease,” “suppressive,” “suppressiveness,” “suppressive soil,” or “plant health.”

Soil-borne diseases by fungal or bacterial pathogens and nematodes cause severe damage in agricultural production worldwide (Strange and Scott, 2005) and soil health assessment without assessing soil-borne diseases can be misleading. Healthy soil, defined using common soil health indicators, can produce unhealthy low-yield crops due to soil-borne diseases (Lazicki and Geisseler, 2021). To ensure healthy crop production, the inclusion of a soil-borne disease management perspective in soil health assessments is critical (van Bruggen and Semenov, 2000; Janvier et al., 2007; Larkin, 2015; Hodson and Lewis, 2016; van Bruggen and Finckh, 2016). However, many pathogens are plant-specific and effective management requires development of crop-, agroecosystem-, or location-specific soil health assessment and management strategies (Miner et al., 2020). While fumigants are widely used to control soil-borne diseases, the negative environmental and human health impacts are spurring development of non-fumigant alternatives for cropping systems worldwide (Labarada, 2008; Porter et al., 2010; López-Aranda et al., 2016; Daugovish et al., 2021).

Agroecology is the integrative study of the food system, encompassing ecological, economic, and social dimensions (Francis et al., 2003; Center for Agroecology, 2021). To create ecologically sound, economically viable, and socially just food systems, agroecology embraces science, practices, and social movements (Gliessman, 2018; Wezel et al., 2020) using transdisciplinary participatory approaches (Méndez et al., 2013). Transdisciplinary approaches value different types of knowledge systems including western scientific, indigenous, and farmer-generated practical knowledge on specific locations (Mendez et al., 2016:5) and co-production of knowledge by stakeholders and experts to realize more just food systems (Anderson et al., 2021).

Though first proposed to connect health between animals, humans, and the environment (Karesh et al., 2012; Wolf, 2015), a novel concept of “One Health” connects soil, plant, animal, human, and ecosystem health through the cycling of diverse microbiomes (Keith et al., 2016; van Bruggen et al., 2019; Altier and Abreo, 2020).

The concept of Integrated Soil Health Management (ISHM) can address management strategies for soil-borne disease and overall soil health. Melakeberhan (2010) used the term “agro-biologically, economically, and ecologically ISHM” that ties nematology and cross-disciplinary gaps for developing agrobiologically sustainable soil health management practices. Manter et al. (2018) argued the importance of underlying soil biology for soil conservation and regeneration. They have proposed a 5-step ISHM approach (knowledge, initial assessment, threshold for action, management, and reassessment) based on the adaptive management framework. However, there has been no examination of ISHM in the context of soil-borne disease management.

Applying the concepts of Integrated Pest Management (IPM) (Cook, 2000) and agroecological transdisciplinary and participatory approaches (Mendez et al., 2016; Anderson et al., 2021), we argue that ISHM and its four components, including farmer's location-specific knowledge and adaptability (Figure 1), offer a framework for developing and implementing a comprehensive site-specific biointensive soil health and soil-borne disease management strategy.

FIGURE 1
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Figure 1. The structure of the integrated soil health management (ISHM) system consists of farmers location-specific knowledge and adaptability, comprehensive soil health diagnostics, a suite of soil health management practices, and decision support tools (optional). Studies on relationships between varying soil health management practices and disease/pest suppression, nutrient uptake, and plant growth will help improve the diagnostic methods and develop actionable thresholds in diagnostics. Rectangular shapes and oval shapes indicate hardware/physical elements and software/intellectual elements of the system, respectively. Roles of decision support tools can be substituted or enhanced by agricultural professionals, consultants, and/or farmer-to-farmer networks (social learning).

We begin with a brief case study review of the history of soil-borne disease management in California strawberries. Then, we contrast this with a history of arthropod pest management to illustrate the unique challenges associated with soil-borne disease management and future directions of soil health research. Lastly, we discuss the ISHM system and its relationship with One Health.

Case Study: History of Soil-Borne Disease Management in California Strawberry

California produces ~90% of strawberries in the US. In 2019, 1.0 million tons of fruits, valued at 2.2 billion dollars, were produced from 14,326 hectares of strawberry fields in the state (California Department of Food and Agriculture, 2021). The large-scale monocultural production of this lucrative crop has evolved dependent on the core technology of pre-plant soil fumigation (Guthman, 2019). Since the 1960s, chemical fumigation using methyl bromide mixed with chloropicrin, was the primary tool to control soil-borne diseases and weeds in California strawberries (Wilhelm et al., 1961; Holmes et al., 2020). Later, methyl bromide was identified as a significant stratospheric ozone-depleting compound by the Montreal Protocol (Ozone Secretariat Team, UNEP, 2020) and was phased out for strawberry production in 2016.

In response, growers increased the use of alternative fumigants, such as chloropicrin and 1,3-dichloropropene, but they lacked effectiveness over the methyl bromide/chloropicrin mixture (Holmes et al., 2020).

The use of fumigants is highly regulated due to their toxicity and high application rates (California Department of Pesticide Regulation (CDPR), 2020) and negative impacts of fumigants on soil health (Dangi et al., 2017) and human health (Gemmill et al., 2013) have been reported. CDPR has documented hundreds of acute illnesses due to accidental exposure for both agricultural workers and populations adjacent to fumigated fields since 2003 (California Department of Pesticide Regulation (CDPR), 2013).

The California Strawberry Commission (CSC) initiated the “Farming without Fumigants” initiative in 2007 (Shennan et al., 2008). Non-fumigant approaches such as anaerobic soil disinfestation (ASD) (Shennan et al., 2018; Muramoto et al., 2020; Rosskopf et al., 2020), crop rotation with disease suppressive crops (Subbarao et al., 2007), use of host plant resistance (Guthman, 2019; Holmes et al., 2020), integration of these techniques (Shennan et al., 2020; Zavatta et al., 2021), substrate production (Thomas et al., 2014), and steaming with a mobile machine (Fennimore and Goodhue, 2016; Xu et al., 2017) have been examined. Overall, however, the adoption of non-fumigant approaches at conventional strawberry fields is yet limited.

Organic strawberry production may have the highest levels of adoption of fumigant alternatives. The acreage of organic strawberries has been gradually increasing since the 1980s (Gliessman and Muramoto, 2010) reaching 1,982 hectares, 13% of total strawberry acreage in California in 2021(California Department of Food and Agriculture (CDFA), 2021). Although typical organic yield is about 60% of the conventional counterpart (Bolda et al., 2016, 2019) disease suppressive strategies such as crop rotation with broccoli, host plant resistance, and ASD, alone or in combination, have supported the growth in organic strawberry acreage.

The recent development of rapid and accurate molecular diagnostic techniques is gradually making “scouting” of soil-borne pathogens a reality. For major lethal soil-borne pathogens in California strawberries, molecular approaches for Verticillium dahliae in plants (Dan et al., 2001) and soil (Bilodeau et al., 2012), Fusarium oxysporum f. sp. fragariae in plants (Burkhardt et al., 2019), and Macrophomina phaseolina in plant and soil (Burkhardt et al., 2018) have been established.

Recently, Lazcano et al. (2021) found that the rhizosphere microbiome plays a role in the resistance to soil-borne pathogens. Strong genotype by environment interactions observed suggests that soil health may also play a role in establishing beneficial plant-microbial interactions.

Lessons From a History of Arthropod Pest Management

A history of arthropod pest management may offer some lessons for the future of soil-borne disease and soil health management. Between the 1940s and 1960s, broad-spectrum, highly toxic insecticides were widely used in arthropod pest management (Carson, 1962) following the motto, “the only good bug is a dead bug.” (Warner, 2007: 141). In the late 1960s to early 1970s, due to “(insecticide) resistance, resurgence of primary pests, upsurges of secondary pests, and overall environmental contamination (Kogan, 1998: 245),” the concept of IPM was developed (Council on Environmental Quality, 1972) recognizing “there are good bugs (beneficial) as well as bad bugs (pests).” In the IPM system, transitioning to biointensive (National Research Council, 1996) or prevention-based IPM (Jacobsen, 1997) as well as redesigning of cropping systems (Hill, 1998) aimed at fostering plant and insect community and population dynamics that self-regulated pest presence and damage. More recently, the extinction of some arthropod species (Kiritani, 2000) and the decline of honeybee colonies (vanEngelsdorp et al., 2009; Ratnieks and Carreck, 2010) has raised awareness of the benefits of arthropod biodiversity and pollinators leading to the realization that “without bugs, we might all be dead.” (Worrall, 2017). In biological control, social learning among farmers, rather than top-down extension, became more critical to implementing and disseminating knowledge-intensive approaches (Fakih et al., 2003; Warner, 2007).

In contrast, for soil-borne disease management in California strawberries, relatively broad-spectrum fumigants are still in use, and the IPM approach (Katan, 2014) is just beginning. The slow transition is partially due to the unique challenges associated with soil-borne disease management. For example, compared to arthropod pests, soil-borne pathogens are microscopic and require specific processes for identification that are still in the nascent stages of development and utilization. Identification and scouting are typically the first step of the IPM approach (Kogan, 1998). Unlike arthropod pest management, there are effectively no post-symptomatic treatments for soil-borne diseases. Instead, currently available treatments are all pre-plant treatments and the availability of non-fumigant alternatives is limited. The complexity and heterogeneity of soil ecosystems, the diversity of soil organisms, and the lack of basic understanding of plant-soil-microbiome interactions have limited a quicker transition to non-fumigant-based IPM approaches (Bardgett and van der Putten, 2014; Mazzola and Freilich, 2017; Thomashow et al., 2019). Further, risks due to the substantial financial investment required in wholesale marketing of high-value horticultural crops hinder the adoption of less proven non-fumigant soil-borne disease management approaches (Chellemi and Porter, 2001; Guthman, 2020).

However, advances in molecular techniques, computational power, and statistics over the last 20 years have rapidly increased our knowledge of soil-plant microbiomes and their functions. Similar to the “discovery” of “good bugs” in arthropod management, we are now understanding the importance of beneficial (Mendes et al., 2013), commensal (Teixeira et al., 2019), and core microbes (Banerjee et al., 2018; Toju et al., 2018). Mechanisms of suppressive soil conditions are a highly active area of research (Schlatter et al., 2017; Duran et al., 2021; Samaddar et al., 2021). To understand plant-soil microbe interactions as a part of the plant defense system, concepts of soil (Lapsansky et al., 2016) and plant memory (Kong et al., 2019), and plant (Han, 2019; Teixeira et al., 2019) and rhizosphere immunity (Wei et al., 2020) have been proposed. As we better understand the soil biome's life cycles, structures, and functions and their relationships with plant health, indicators and thresholds of beneficial soil microbes and soil microbial communities may be developed for specific crops or agroecosystems (Blundell et al., 2020).

European Union (EU) has one of the world's most stringent fumigant regulations and is leading in the development of the IPM approach for soil-borne disease management. They developed “Soil Health Strategy Actions” (The Agricultural European Innovation Partnership (EIP-AGRI) Focus Group, 2015) consisting of prevention (certified seed, sanitation, and weed control), monitoring (soil sampling, bioassay), crop rotation (frequency, sequence, green manure, resistant varieties), and additional measures (grafting, biological control agents, biofumigation, ASD, organic amendments, solarization, etc.).

Integrated Soil Health Management System, Agroecosystem Health and One Health

We propose that ISHM, as a science and practice, with social movement advocacy for non-toxic agriculture, may evolve similarly to IPM for arthropod pest management; toward biointensive management, increasing prioritization of the role of beneficial organisms, and redesigning cropping systems and cultural practices that prevent soil-borne diseases and induce sustained soil and plant health. At the same time, ISHM is more than a simple application of integrated “soil-borne disease” management, it also encompasses soil's many other functions by improving overall soil health using transdicisplinary participatory approaches.

The proposed ISHM system in this context consists of 4 components (Figure 1). First, a comprehensive soil health diagnostic system created by integrating molecular approaches for quantifying pathogens, beneficials, and soil microbial indicators and their thresholds, developed with an existing soil health measurement system measuring physical, chemical, and biological soil properties for assessing soils' other functions such as nutrient cycling, water retention, and carbon transformation (Andrews et al., 2004; Moebius-Clune et al., 2016; Norris et al., 2020). The diagnostic system will determine the disease potential both from the pathogens density in the soil relative to their economic thresholds and the disease suppressiveness of the soil toward target pathogens evaluated by its biotic and abiotic properties (Postma et al., 2014; Schlatter et al., 2017). To ensure healthy crop production, monitoring of plant health indicators (e.g., nutrients and chlorophyll contents, mycorrhiza and endophyte colonization rates, pathogen infection rates, etc.) will complement the soil health assessment during the cropping season.

EU (Clarkson et al., 2015) and Australia lead molecular plant-pathogen diagnostics services. PREDICTA® by the South Australian Research and Development Institute (Stirling et al., 2016; Government of South Australia, 2021), for example, is a fee-based public service for cereals, potatoes, and research, in which more than 10 pathogens and some beneficial microbes are quantified. The cost of quantifying soil microorganisms may hinder accessibility and affordability among diverse stakeholders. Development of portable, accurate, and easy to operate sequencers (Baldi and La Porta, 2020; Cunha et al., 2020) may allow farmers to determine soil and plant biomes in the field as “point-of-care” and may reduce the costs of diagnostics and empower farmers (Clarkson et al., 2015).

This information will then be integrated with farmers' location-specific knowledge and adaptability. Although often overlooked and underappreciated, farmers' location-specific knowledge gained from day-to-day fieldwork and observations and their adaptability to dynamic agroecosystems and climate change (Stockdale, 2011) is central to ISHM. Integration of scientific data obtained by diagnostics and farmers' experiential location-specific knowledge can be synergistic (Lobry de Bruyn and Andrews, 2016; Šumane et al., 2018). Dialogue between farmers and scientists centers farmers as an active player in examining, fine-tuning, and scaling-out agroecological knowledge and practices (Blundell et al., 2020; Anderson et al., 2021). Such participatory and transdisciplinary approaches mobilize knowledge for social change and engage stakeholders in research (Mendez et al., 2016).

The third component is a suite of soil health management practices (SHMPs) known to improve soil health. As seen in the EU program, various SHMPs including practices for prevention and enhancing disease suppression via general or specific suppressiveness (see Figure 1. e.g., applying organic amendments, cover cropping, crop rotation, using host resistance) (Abawi and Widmer, 2000; Raaijmakers et al., 2009; Hiddink et al., 2010; Larkin, 2015; Rosskopf et al., 2020) are integrated to tailor a site-specific soil-borne disease and soil health management strategy. A more intensive approach such as ASD and steaming is applied on an “as-needed” basis, depending on the soil health diagnostic result.

Lastly, decision support tools will assist growers in developing site-specific soil health management strategies based on their goals, knowledge, environmental conditions (e.g., soil type, climate, etc.), available SHMPs, results of soil health diagnostics, and other factors. Figure 2 illustrates how ISHM is embedded in agroecosystem management and how it relates to the health of soil, plants, animals, humans, and agroecosystems and the concept of One Health.

FIGURE 2
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Figure 2. Agroecosystem management and the concept of One Health. Integrated soil health management is embedded in this system. Agroecological principles include recycling, input reduction, soil health, animal health, biodiversity, synergy, economic diversification, co-creation of knowledge, social values and diets, fairness, connectivity, land and natural resource governance, and participation, according to a recent review by Wenzel et al. (2020). Habitat management and diversification have spatial (farm and landscape levels) and temporal dimensions. Environmental health includes the health of air and water. See Figure 1 for soil health diagnostics, decision support tools, and soil health management practices. Modified from Altieri and Nicholls (2003).

Discussion

Although ISHM provides a framework, there are many knowledge gaps in the components parts. Primary research needs for developing ISHM include utilizing mechanistic models in plants-soil microbe functions such as soil suppressiveness, plant immunity, nutrient uptake (Liu et al., 2016; Trivedi et al., 2017), better chemical and biological characterization of organic amendments and crop residues, and their relationships with soil-borne disease suppressiveness (Bonanomi et al., 2018; Subbarao et al., 2020), increased efficacy of plant growth-promoting microbes in soil-borne disease suppression and nutrient uptake in field conditions (Rosier et al., 2018; Hestrin et al., 2019), and development of crop cultivars with ability to modify their rhizosphere microbiome for their benefits (Berg et al., 2016; Mendes et al., 2018).

ISHM is characterized as a location-specific and knowledge-intensive approach (Jacobsen, 1997), contrasted with the location-general and chemical-intensive fumigation and industrial farming approach. However, the transition to knowledge-intensive systems can present significant obstacles for farmers. As it worked in biocontrol (Warner, 2007), social learning, as seen in farmer-to-farmer networks, has facilitated the implementation and extension of knowledge-intensive soil health management (De Bruyn et al., 2017; Stockdale et al., 2019; Wick et al., 2019; Skaalsveen et al., 2020). Policies and extension activities that support such a process and the adoption of ISHM will be necessary for the greater engagement in the co-development of ISHM with and among stakeholders.

ISHM is additionally important as impacts of soil health may go beyond plant health. Indeed, our understanding of the direct and indirect effects of soil health on human health through microbiomes (Wall et al., 2015; Stegen et al., 2018; Samaddar et al., 2021) is increasing. The “One Health” concept suggests the interconnectedness of soil, plant, animal, human, and ecosystem health through microbiome cycling (van Bruggen et al., 2019, Figure 2). More than 70 years ago, Sir Albert Howard, an early student, and advocate of organic farming (Heckman, 2006), wrote, “The birthright of all living things is health. This law is true for soil, plant, animal, and man: the health of these four is one connected chain. Any weakness or defect in the health of any earlier link in the chain is carried on to the next succeeding links, until it reaches the last, mainly, man.” (Howard, 1947). Although our understanding is yet at its infancy, future research on microbiome cycling and nutrient cycling (Altieri and Nicholls, 2003; Datnoff et al., 2007) may hold the key to better understanding the chains connecting healthy soils to plants, animals, humans, and ecosystems.

Data Availability Statement

The original contributions presented in the study are included in the article, further inquiries can be directed to the corresponding author/s.

Author Contributions

JM: conceptualization and draft manuscript preparation. DP, JP, and DW: critically revised it, adding conceptual material and clarity. All authors contributed to the article and approved the submitted version.

Funding

The University of California Agriculture and Natural Resources and the University of California Santa Cruz provided funding for this article. The author did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Conflict of Interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Publisher's Note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

Acknowledgments

The authors are grateful to reviewers for their constructive feedback on a previous version of this manuscript. We also thank Prof. Stacy Philpott, Prof. Timothy Bowles, Prof. Carol Shennan, Emeritus Prof. Stephen R. Gliessman, and Mr. Scott Park for their support, inputs, and inspiration in preparing this manuscript.

References

Abawi, G. S., and Widmer, T. L. (2000). Impact of soil health management practices on soil-borne pathogens, nematodes and root diseases of vegetable crops. Agric. Ecosyst. Environ. Appl. Soil Ecol. 15, 37–47. doi: 10.1016/S0929-1393(00)00070-6

CrossRef Full Text | Google Scholar

Altier, N., and Abreo, E. (2020). One health considerations in the International Year of Plant Health. Agrociencia-Uruguay 24, 1–14. doi: 10.31285/AGRO.24.422

CrossRef Full Text | Google Scholar

Altieri, M. A., and Nicholls, C. I. (2003). Soil fertility management and insect pests: harmonizing soil and plant health in agroecosystems. Soil Tillage Res. 72, 203–211. doi: 10.1016/S0167-1987(03)00089-8

CrossRef Full Text | Google Scholar

Anderson, C. R., Bruil, J., Chappell, M. J., Kiss, C., and Pimbert, M. P. (2021). Agroecology Now!: Transformations Towards More Just and Sustainable Food Systems. Basingstoke: Palgrave Macmillan. doi: 10.1007/978-3-030-61315-0

CrossRef Full Text | Google Scholar

Andrews, S. S., Karlen, D. L., and Cambardella, C. A. (2004). The soil management assessment framework: a quantitative soil quality evaluation method. Soil Sci. Soc. Am. J. 68, 1945–1962. doi: 10.2136/sssaj2004.1945

PubMed Abstract | CrossRef Full Text | Google Scholar

Baldi, P., and La Porta, N. (2020). Molecular approaches for low-cost point-of-care pathogen detection in agriculture and forestry. Front. Plant Sci. 11, 3389. doi: 10.3389/fpls.2020.570862

PubMed Abstract | CrossRef Full Text | Google Scholar

Banerjee, S., Schlaeppi, K., and van der Heijden, M. G. A. (2018). Keystone taxa as drivers of microbiome structure and functioning. Nat. Rev. Microbiol. 16, 567–576. doi: 10.1038/s41579-018-0024-1

PubMed Abstract | CrossRef Full Text | Google Scholar

Bardgett, R. D., and van der Putten, W. H. (2014). Belowground biodiversity and ecosystem functioning. Nature 515, 505–511. doi: 10.1038/nature13855

PubMed Abstract | CrossRef Full Text | Google Scholar

Berg, G., Rybakova, D., Grube, M., and Koberl, M. (2016). The plant microbiome explored: implications for experimental botany. J. Exp. Bot. 67, 995–1002. doi: 10.1093/jxb/erv466

PubMed Abstract | CrossRef Full Text | Google Scholar

Bilodeau, G. J., Koike, S. T., Uribe, P., and Martin, F. N. (2012). Development of an assay for rapid detection and quantification of Verticillium dahliae in soil. Phytopathology 102, 331–343. doi: 10.1094/PHYTO-05-11-0130

PubMed Abstract | CrossRef Full Text | Google Scholar

Blundell, R., Schmidt, J. E., Igwe, A., Cheung, A. L., Vannette, R. L., Gaudin, A. C. M., et al. (2020). Organic management promotes natural pest control through altered plant resistance to insects. Nature Plants 6, 483–491. doi: 10.1038/s41477-020-0656-9

PubMed Abstract | CrossRef Full Text | Google Scholar

Bolda, M., Tourte, L., Murdock, J., and Sumner, D. A. (2016). “Sample costs to produce and harvest strawberries: Central coast, Santa Cruz, Monterey, and San Benito Counties,” in University of California Cooperative Extension. Davis, CA, 20.

Google Scholar

Bolda, M., Tourte, L., Murdock, J., and Sumner, D. A. (2019). “Sample costs to produce and harvest organic strawberries: Central coast, Santa Cruz, Monterey, and San Benito Counties,” in University of California Cooperative Extension. Davis, CA, 19.

Google Scholar

Bonanomi, G., Lorito, M., Vinale, F., and Woo, S. L. (2018). “Organic amendments, beneficial microbes, and soil microbiota: Toward a unified framework for disease suppression,” in Annual Review of Phytopathology, Vol. 56, eds J. E. Leach, and S. E. Lindow, (San Mateo, CA), 1–20. doi: 10.1146/annurev-phyto-080615-100046

PubMed Abstract | CrossRef Full Text | Google Scholar

Bünemann, E. K., Bongiorno, G., Bai, Z. G., Creamer, R. E., De Deyn, G., de Goede, R., et al. (2018). Soil quality - a critical review. Soil Biol. Biochem. 120, 105–125. doi: 10.1016/j.soilbio.2018.01.030

CrossRef Full Text | Google Scholar

Burkhardt, A., Henry, P. M., Koike, S. T., Gordon, T. R., and Martin, F. (2019). Detection of Fusarium oxysporum f. sp. fragariae from infected strawberry plants. Plant Dis. 103, 1006–1013. doi: 10.1094/PDIS-08-18-1315-RE

PubMed Abstract | CrossRef Full Text | Google Scholar

Burkhardt, A., Ramon, M. L., Smith, B., Koike, S. T., and Martin, F. (2018). Development of molecular methods to detect Macrophomina phaseolina from strawberry plants and soil. Phytopathology 108, 1386–1394. doi: 10.1094/PHYTO-03-18-0071-R

PubMed Abstract | CrossRef Full Text | Google Scholar

California Department of Food Agriculture (CDFA) (2021). California Agricultural Statistical Review 2019-2020. Sacramento, CA: California Department of Food Agriculture (CDFA). Available online at: https://www.cdfa.ca.gov/Statistics/ (accessed December 19, 2021).

Google Scholar

California Department of Pesticide Regulation (CDPR) (2013). Nonfumigant Strawberry Production Working Group Action Plan. Sacramento, CA, 34. Available online at: https://www.cdpr.ca.gov/docs/pressrls/2013/130409.htm (accessed on March 11, 2022).

Google Scholar

California Department of Pesticide Regulation (CDPR) (2020). California code of regulations (Title 3. Food and Agriculture), Division 6. Pesticides and pest control operations, Chapter 3. Pest control operations, Subchapter 3. Pesticide worker safety, Article 4. Fumigation. Available online at: https://www.cdpr.ca.gov/docs/legbills/calcode/030304.htm (accessed December 19, 2021).

Google Scholar

California Strawberry Commission (CSC) (2021). Acreage Survey – Update. Available online at: https://calstrawberry1.sharepoint.com/:b:/r/sites/IndustryPortal-Landing/Market%20Data/Acreage%20Surveys/2021%20Acreage%20Survey.pdf?csf=1&web=1&e=iHMsMg (accessed Decemeber 19, 2021).

Google Scholar

Carson, R. (1962). Houghton Mifflin. Boston, MA: Silent Spring.

Google Scholar

Center for Agroecology (2021). What is Agroecology?. Available online at: https://agroecology.ucsc.edu/about/index.html (accessed December 19, 2021)

Google Scholar

Chellemi, D. O., and Porter, I. J. (2001). The role of plant pathology in understanding soil health and its application to production agriculture. Austral. Plant Pathol. 30, 103–109. doi: 10.1071/AP01008

CrossRef Full Text | Google Scholar

Clarkson, J., Debode, J., Furlan, L., Neilson, R., Wallenhammer, A., and Zahrl, J. (2015). Mini-Paper - Monitoring of Soil-Borne Pathogens (fungi, protists and nematodes) and Soil Test. Focus Group Soil-Borne Diseases, EIP-AGRI. Brussels, Belgium. Available online at: https://ec.europa.eu/eip/agriculture/sites/agri-eip/files/7_eip_sbd_mp_monitoring_final_0.pdf (accessed on March 11, 2022).

Google Scholar

Cook, R. J. (2000). Advances in plant health management in the twentieth century. Annu. Rev. Phytopathol. 38, 95–116. doi: 10.1146/annurev.phyto.38.1.95

PubMed Abstract | CrossRef Full Text | Google Scholar

Council on Environmental Quality (1972). Integrated Pest Management. Washington, DC: Council on Environmental Quality, 41.

Google Scholar

Cunha, E. N., de Souza, M. F. B., Lanza, D. C. F., and Lima, J. (2020). A low-cost smart system for electrophoresis-based nucleic acids detection at the visible spectrum. PLoS ONE 15:e0240536. doi: 10.1371/journal.pone.0240536

PubMed Abstract | CrossRef Full Text | Google Scholar

Dan, H., Ali-Khan, S. T., and Robb, J. (2001). Use of quantitative PCR diagnostics to identify tolerance and resistance to Verticillium dahliae in potato. Plant Dis. 85:700–705. doi: 10.1094/PDIS.2001.85.7.700

PubMed Abstract | CrossRef Full Text | Google Scholar

Dangi, S. R., Tirado-Corbala, R., Gerik, J., and Hanson, B. D. (2017). Effect of long-term continuous fumigation on soil microbial communities. Agronomy-Basel 7, 37. doi: 10.3390/agronomy7020037

CrossRef Full Text | Google Scholar

Datnoff, L. E., Elmer, W. H., and Huber, D. M. (2007). Mineral Nutrition and Plant Disease. St. Paul, MN: American Phytopathological Society.

Google Scholar

Daugovish, O., Knapp, S., Gordon, T., Fennimore, S., Muramoto, J., and Bolda, M. (2021). Soil pest management in current California strawberry production: a review. Acta Hortic. 1309, 701–709. doi: 10.17660/ActaHortic.2021.1309.101

CrossRef Full Text | Google Scholar

De Bruyn, L. L., Jenkins, A., and Samson-Liebig, S. (2017). Lessons learnt: sharing soil knowledge to improve land management and sustainable soil use. Soil Sci. Soc. Am. J. 81, 427–438. doi: 10.2136/sssaj2016.12.0403

CrossRef Full Text | Google Scholar

Duran, P., Tortella, G., Sadowsky, M. J., Viscardi, S., Javier Barra, P., and de la Luz Mora, M. (2021). Engineering multigenerational host-modulated microbiota against soil-borne pathogens in response to global climate change. Biology-Basel 10, 865. doi: 10.3390/biology10090865

PubMed Abstract | CrossRef Full Text | Google Scholar

Fakih, M., Rahardjo, T., and Pimbert, M. P. (2003). Community Integrated Pest Management in Indonesia: Institutionalising Participation and People Centred Approaches. London: IIED. Available online at: https://pubs.iied.org/9293iied

Google Scholar

Fennimore, S. A., and Goodhue, R. E. (2016). Soil disinfestation with steam: a review of economics, engineering, and soil pest control in California Strawberry. Int. J. Fruit Sci. 16, 71–83. doi: 10.1080/15538362.2016.1195312

CrossRef Full Text | Google Scholar

Francis, C., Lieblein, G., Gliessman, S., Breland, T. A., Creamer, N., Harwood, R., et al. (2003). Agroecology: the ecology of food systems. J. Sustain. Agric. 22, 99–118. doi: 10.1300/J064v22n03_10

CrossRef Full Text | Google Scholar

Gemmill, A., Gunier, R., Bradman, A., Eskenazi, B., and Harley, K. (2013). Residential proximity to methyl bromide use and birth outcomes in an agricultural population in California. Environ. Health Perspect. 121, 737–743. doi: 10.1289/ehp.1205682

PubMed Abstract | CrossRef Full Text | Google Scholar

Gliessman, S. R. (2018). Defining agroecology. Agroecol. Sustain. Food Syst. 42, 599–600. doi: 10.1080/21683565.2018.1432329

CrossRef Full Text | Google Scholar

Gliessman, S. R., and Muramoto, J. (2010). “California (USA) - The Conversion of strawberry production,” in The Conversion to Sustainable Agriculture: Principles, Processes, and Practices, eds S. R. Gliessman, and M. E. Rosemeyer (Baca Raton, FL: CRC press), 117–131. doi: 10.1201/9781420003598-c6

CrossRef Full Text | Google Scholar

Government of South Australia (2021). Molecular Diagnostics (PREDICTA). Available online at: https://pir.sa.gov.au/research/services/molecular_diagnostics (accessed December 19, 2021)

Google Scholar

Guthman, J. (2019). Wilted: Pathogens, Chemicals, and the Fragile Future of the Strawberry Industry. Oakland, CA: University of California Press. doi: 10.1525/9780520973343

CrossRef Full Text | Google Scholar

Guthman, J. (2020). Strawberry growers are unlikely to forgo soil fumigation with disease-resistant cultivars alone. Calif. Agric. 74, 138–143. doi: 10.3733/ca.2020a0021

CrossRef Full Text | Google Scholar

Han, G. Z. (2019). Origin and evolution of the plant immune system. New Phytol. 222, 70–83. doi: 10.1111/nph.15596

PubMed Abstract | CrossRef Full Text | Google Scholar

Heckman, J. (2006). A history of organic farming: transitions from Sir Albert Howard's War in the soil to USDA National Organic Program. Renew. Agric. Food Syst. 21, 143–150. doi: 10.1079/RAF2005126

CrossRef Full Text | Google Scholar

Hestrin, R., Hammer, E. C., Mueller, C. W., and Lehmann, J. (2019). Synergies between mycorrhizal fungi and soil microbial communities increase plant nitrogen acquisition. Commun. Biol. 2, 233. doi: 10.1038/s42003-019-0481-8

PubMed Abstract | CrossRef Full Text | Google Scholar

Hiddink, G. A., Termorshuizen, A. J., and van Bruggen, A. H. C. (2010). “Mixed cropping and suppression of soil-borne diseases,” in Genetic Engineering, Biofertilisation, Soil Quality and Organic Farming, ed E. Lichtfouse, (Dordrecht; Heidelberg; London; New York, NY: Springer), 119–146. doi: 10.1007/978-90-481-8741-6_5

CrossRef Full Text | Google Scholar

Hill, S. B. (1998). Redesigning agroecosystems for environmental sustainability: a deep systems approach. Syst. Res. Behav. Sci. 15, 391–402. doi: 10.1002/(SICI)1099-1743(1998090)15:5<391::AID-SRES266>3.0.CO;2-0

CrossRef Full Text | Google Scholar

Hodson, A., and Lewis, E. (2016). Managing for soil health can suppress pests. Calif. Agric. 70, 137–141. doi: 10.3733/ca.2016a0005

PubMed Abstract | CrossRef Full Text | Google Scholar

Holmes, G. J., Mansouripour, S. M., and Hewavitharana, S. S. (2020). Strawberries at the crossroads: management of soil-borne diseases in California without methyl bromide. Phytopathology 110, 956–968. doi: 10.1094/PHYTO-11-19-0406-IA

PubMed Abstract | CrossRef Full Text | Google Scholar

Howard, S. A. (1947). The Soil and Health: A Study of Organic Agriculture. New York, NY: Devin-Adair.

Google Scholar

Jacobsen, B. J. (1997). Role of plant pathology in integrated pest management. Annu. Rev. Phytopathol. 35, 373–391. doi: 10.1146/annurev.phyto.35.1.373

PubMed Abstract | CrossRef Full Text | Google Scholar

Janvier, C., Villeneuve, F., Alabouvette, C., Edel-Hermann, V., Mateille, T., and Steinberg, C. (2007). Soil health through soil disease suppression: which strategy from descriptors to indicators? Soil Biol. Biochem. 39, 1–23. doi: 10.1016/j.soilbio.2006.07.001

CrossRef Full Text | Google Scholar

Karesh, W. B., Dobson, A., Lloyd-Smith, J. O., Lubroth, J., Dixon, M. A., Bennett, M., et al. (2012). Ecology of zoonoses: natural and unnatural histories. Lancet 380, 1936–1945. doi: 10.1016/S0140-6736(12)61678-X

PubMed Abstract | CrossRef Full Text | Google Scholar

Katan, J. (2014). Integrated pest management in connection with soil disinfestation. Acta Hortic. 1044, 19–28. doi: 10.17660/ActaHortic.2014.1044.1

CrossRef Full Text | Google Scholar

Keith, A. M., Schmidt, O., and McMahon, B. J. (2016). Soil stewardship as a nexus between Ecosystem Services and One Health. Ecosyst. Serv. 17, 40–42. doi: 10.1016/j.ecoser.2015.11.008

CrossRef Full Text | Google Scholar

Kibblewhite, M. G., Ritz, K., and Swift, M. J. (2008). Soil health in agricultural systems. Philos. Trans. R Soc. Lond. B Biol. Sci. 363, 685–701. doi: 10.1098/rstb.2007.2178

PubMed Abstract | CrossRef Full Text | Google Scholar

Kiritani, K. (2000). Integrated biodiversity management in paddy fields: shift of paradigm from IPM toward IBM. Integrated Pest Manage. Rev. 5, 175–183. doi: 10.1023/A:1011315214598

CrossRef Full Text | Google Scholar

Kogan, M. (1998). Integrated pest management: historical perspectives and contemporary developments. Annu. Rev. Entomol. 43, 243–270. doi: 10.1146/annurev.ento.43.1.243

PubMed Abstract | CrossRef Full Text | Google Scholar

Kong, H. G., Song, G. C., and Ryu, C. M. (2019). Inheritance of seed and rhizosphere microbial communities through plant-soil feedback and soil memory. Environ. Microbiol. Rep. 11, 479–486. doi: 10.1111/1758-2229.12760

PubMed Abstract | CrossRef Full Text | Google Scholar

Labarada, R. (2008). Workshop on Non-chemical Alternatives to Replace Methyl Bromide as a Soil Fumigant: REPORT 26–28 June (2007). Budapest: FAO, 136. Available online at: https://www.fao.org/3/i0178e/i0178e.pdf

Google Scholar

Lapsansky, E. R., Milroy, A. M., Andales, M. J., and Vivanco, J. M. (2016). Soil memory as a potential mechanism for encouraging sustainable plant health and productivity. Curr. Opin. Biotechnol. 38, 137–142. doi: 10.1016/j.copbio.2016.01.014

PubMed Abstract | CrossRef Full Text | Google Scholar

Larkin, R. P. (2015). “Soil health paradigms and implications for disease management,” in Annual Review of Phytopathology, Vol. 53, ed N. K. Van Alfen, (San Mateo, CA), 199–221. doi: 10.1146/annurev-phyto-080614-120357

PubMed Abstract | CrossRef Full Text | Google Scholar

Lazcano, C., Boyd, E., Holmes, G., Hewavitharana, S., Pasulka, A., and Ivors, K. (2021). The rhizosphere microbiome plays a role in the resistance to soil-borne pathogens and nutrient uptake of strawberry cultivars under field conditions. Sci. Rep. 11, 3188. doi: 10.1038/s41598-021-82768-2

PubMed Abstract | CrossRef Full Text | Google Scholar

Lazicki, P., and Geisseler, D. (2021). Relating indicators to soil health functions in conventional and organic Mediterranean cropping systems. Soil Sci. Soc. Am. J. 85, 1843–1857. doi: 10.1002/saj2.20279

CrossRef Full Text | Google Scholar

Lehman, R. M., Cambardella, C. A., Stott, D. E., Acosta-Martinez, V., Manter, D. K., Buyer, J. S., et al. (2015). Understanding and enhancing soil biological health: The solution for reversing soil degradation. Sustainability 7, 988–1027. doi: 10.3390/su7010988

CrossRef Full Text | Google Scholar

Liu, X. J., Zhang, S. T., Jiang, Q. P., Bai, Y. N., Shen, G. H., Li, S. L., et al. (2016). Using community analysis to explore bacterial indicators for disease suppression of tobacco bacterial wilt. Sci. Rep. 6, 36773. doi: 10.1038/srep36773

PubMed Abstract | CrossRef Full Text | Google Scholar

Lobry de Bruyn, L., and Andrews, S. (2016). Are Australian and United States farmers using soil information for soil health management? Sustainability 8, 304. doi: 10.3390/su8040304

CrossRef Full Text | Google Scholar

López-Aranda, J. M., Domínguez, P., Miranda, L., de los Santos, B., Talavera, M., Daugovish, O., et al. (2016). Fumigant use for strawberry production in Europe: the current landscape and solutions. Int. J. Fruit Sci. 16, 1–15. doi: 10.1080/15538362.2016.1199995

CrossRef Full Text | Google Scholar

Manter, D. K., Delgado, J. A., and Moore-Kucera, J. (2018). “Integrated soil health management: a framework for soil conservation and regeneration,” in Managing Soil Health for Sustainable Agriculture, Vol. 1, ed D. Reicosky (Philadelphia, PA: Fundamentals), 69–87. doi: 10.19103/AS.2017.0033.05

CrossRef Full Text | Google Scholar

Mazzola, M., and Freilich, S. (2017). Prospects for biological soil-borne disease control: application of indigenous versus synthetic microbiomes. Phytopathology 107, 256–263. doi: 10.1094/PHYTO-09-16-0330-RVW

PubMed Abstract | CrossRef Full Text | Google Scholar

Melakeberhan, H. (2010). Assessing cross-disciplinary efficiency of soil amendments for agro-biologically, economically, and ecologically integrated soil health management. J. Nematol. 42, 73–77.

PubMed Abstract | Google Scholar

Mendes, L. W., Mendes, R., Raaijmakers, J. M., and Tsai, S. M. (2018). Breeding for soil-borne pathogen resistance impacts active rhizosphere microbiome of common bean. ISME J. 12, 3038–3042. doi: 10.1038/s41396-018-0234-6

PubMed Abstract | CrossRef Full Text | Google Scholar

Mendes, R., Garbeva, P., and Raaijmakers, J. M. (2013). The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiol. Rev. 37, 634–663. doi: 10.1111/1574-6976.12028

PubMed Abstract | CrossRef Full Text | Google Scholar

Mendez, V.E., Bacon, C.M., Cohen, R., and Gliessman, S.R. (Eds.) (2016). Agroecology: A Transdisciplinary, Participatory, and Action-Oriented Approach. (Boca Raton, FL: Taylor and Francis) doi: 10.1201/b19500

CrossRef Full Text | Google Scholar

Méndez, V. E., Bacon, C. M., and Cohen, R. (2013). Agroecology as a transdisciplinary, participatory, and action-oriented approach. Agroecol. Sustain. Food Syst. 37:3–18. doi: 10.1080/10440046

CrossRef Full Text | Google Scholar

Miner, G. L., Delgado, J. A., Ippolito, J. A., and Stewart, C. E. (2020). Soil health management practices and crop productivity. Agric. Environ. Lett. 5, e20023. doi: 10.1002/ael2.20023

CrossRef Full Text | Google Scholar

Moebius-Clune, B. N., Moebius-Clune, D. J., Gugino, B. K., Idowu, O. J., Schindelbeck, R. R., Ristow, A. J., et al. (2016). Comprehensive Assessment of Soil Health - The Cornell Framework Manual, Edition 3.1. Geneva, NY: Cornell University.

Google Scholar

Muramoto, J., Shennan, C., Mazzola, M., Wood, T., Miethke, E., Resultay, E., et al. (2020). Use of a summer cover crop as a partial carbon source for anaerobic soil disinfestation in coastal California. Acta Hortic. 1270, 37–44. doi: 10.17660/ActaHortic.2020.1270.4

CrossRef Full Text | Google Scholar

National Research Council (1996). Ecologically Based Pest Management: New Solutions for a New Century. Washington, DC: The National Academies Press.

Google Scholar

Norris, C. E., Bean, G. M., Cappellazzi, S. B., Cope, M., Greub, K. L. H., Liptzin, D., et al. (2020). Introducing the North American project to evaluate soil health measurements. Agron. J. 112, 3195–3215. doi: 10.1002/agj2.20234

CrossRef Full Text | Google Scholar

Orgiazzi, A., Bardgett, R. D., Barrios, E., Behan-Pelletier, V., Briones, M. J. I., Chotte, J.-L., et al. (2016). Global Soil Biodiversity Atlas. Luxembourg: Publications Office of the European Union.

Google Scholar

Ozone Secretariat Team, UNEP. (2020). The Montreal Protocol on Substances that Deplete the Ozone Layer (the online edition. Available online at: https://ozone.unep.org/treaties/montreal-protocol-substances-deplete-ozone-layer/introduction). Ozone Secretariat, The Secretariat for the Vienna Convention for the Protection of the Ozone Layer and for the Montreal Protocol on Substances that Deplete the Ozone Layer, United Nations Environment Programme.

Google Scholar

Porter, I., Pizano, M., Besri, M., Mattner, S. W., and Fraser, P. (2010). Progress in the global phase out of methyl bromide and the relative effectiveness of soil disinfestation strategies. Acta Hortic. 883, 59–66. doi: 10.17660/ActaHortic.2010.883.4

CrossRef Full Text | Google Scholar

Postma, J., Schilder, M. T., and Stevens, L. H. (2014). The Potential of organic amendments to enhance soil suppressiveness against rhizoctonia solani disease in different soils and crops. Acta Hortic. 1044, 127–132. doi: 10.17660/ActaHortic.2014.1044.14

CrossRef Full Text | Google Scholar

Raaijmakers, J. M., Paulitz, T. C., Steinberg, C., Alabouvette, C., and Moënne-Loccoz, Y. (2009). The rhizosphere: a playground and battlefield for soil-borne pathogens and beneficial microorganisms. Plant Soil 321, 341–361. doi: 10.1007/s11104-008-9568-6

CrossRef Full Text | Google Scholar

Ratnieks, F. L. W., and Carreck, N. L. (2010). Clarity on honey bee collapse? Science 327, 152–153. doi: 10.1126/science.1185563

PubMed Abstract | CrossRef Full Text | Google Scholar

Rosier, A., Medeiros, F. H. V., and Bais, H. P. (2018). Defining plant growth promoting rhizobacteria molecular and biochemical networks in beneficial plant-microbe interactions. Plant Soil 428, 35–55. doi: 10.1007/s11104-018-3679-5

CrossRef Full Text | Google Scholar

Rosskopf, E., Gioia, F. D., Hong, J. C., Pisani, C., and Kokalis-Burelle, N. (2020). Organic amendments for pathogen and nematode control. Annu. Rev. Phytopathol. 58, 277–311. doi: 10.1146/annurev-phyto-080516-035608

PubMed Abstract | CrossRef Full Text | Google Scholar

Samaddar, S., Karp, D. S., Schmidt, R., Devarajan, N., McGarvey, J. A., Pires, A. F. A., et al. (2021). Role of soil in the regulation of human and plant pathogens: soils' contributions to people. Philos. Trans. R. Soc. B: Biol. Sci. 376, 20200179. doi: 10.1098/rstb.2020.0179

PubMed Abstract | CrossRef Full Text | Google Scholar

Schlatter, D., Kinkel, L., Thomashow, L., Weller, D., and Paulitz, T. (2017). Disease suppressive soils: new insights from the soil microbiome. Phytopathology 107, 1284–1297. doi: 10.1094/PHYTO-03-17-0111-RVW

PubMed Abstract | CrossRef Full Text | Google Scholar

Shennan, C., Muramoto, J., Baird, G., Zavatta, M., Nobua, B., and Mazzola, M. (2020). Effects of crop rotation, anaerobic soil disinfestation, and mustard seed meal on disease severity and organic strawberry production in California. Acta Hortic. 1270, 63–70. doi: 10.17660/ActaHortic.2020.1270.7

CrossRef Full Text | Google Scholar

Shennan, C., Muramoto, J., Koike, S., Baird, G., Fennimore, S., Samtani, J., et al. (2018). Anaerobic soil disinfestation is an alternative to soil fumigation for control of some soil-borne pathogens in strawberry production. Plant Pathol. 67, 51–66. doi: 10.1111/ppa.12721

CrossRef Full Text | Google Scholar

Shennan, C., Muramoto, J., Koike, S. T., and Daugovish, O. (2008). “Optimizing anaerobic soil disinfestation for non-fumigated strawberry production in California,” in California Strawberry Commission Annual Production Research Report 2008-2009. Watsonville, CA: California Strawberry Commission, 113–121.

Google Scholar

Skaalsveen, K., Ingram, J., and Urquhart, J. (2020). The role of farmers' social networks in the implementation of no-till farming practices. Agric. Syst. 181, 1–14. doi: 10.1016/j.agsy.2020.102824

CrossRef Full Text | Google Scholar

Stegen, J. C., Bottos, E. M., and Jansson, J. K. (2018). A unified conceptual framework for prediction and control of microbiomes. Curr. Opin. Microbiol. 44, 20–27. doi: 10.1016/j.mib.2018.06.002

PubMed Abstract | CrossRef Full Text | Google Scholar

Stirling, G. R., Hayden, H., Pattison, T., and Stirling, M. (2016). Soil Health, Soil Biology, Soil-Borne Diseases and Sustainable Agriculture: A Guide. Clayton, VIC: CSIRO Publishing. doi: 10.1071/9781486303052

CrossRef Full Text | Google Scholar

Stockdale, E. (2011). “Organic farming: pros and cons for soil health and climate change,” in Soil Health and Climate Change, eds B. P. Singh, A. L. Cowie, and K. Y. Chan (Berlin: Springer Berlin Heidelberg), 317–343. doi: 10.1007/978-3-642-20256-8_14

CrossRef Full Text | Google Scholar

Stockdale, E. A., Griffiths, B. S., Hargreaves, P. R., Bhogal, A., Crotty, F. V., and Watson, C. A. (2019). Conceptual framework underpinning management of soil health-supporting site-specific delivery of sustainable agro-ecosystems. Food Energy Security 8, 1–18. doi: 10.1002/fes3.158

CrossRef Full Text | Google Scholar

Stott, D. E. (2019). Recommended Soil Health Indicators and Associated Laboratory Procedures. Soil health technical note No. 430-03. US Department of Agriculture Natural Resources Conservation Service, Washington DC.

Google Scholar

Strange, R. N., and Scott, P. R. (2005). Plant disease: a threat to global food security. Annu. Rev. Phytopathol. 43, 83–116. doi: 10.1146/annurev.phyto.43.113004.133839

PubMed Abstract | CrossRef Full Text | Google Scholar

Subbarao, K. V., Inderbitzin, P., Puri, K. D., and Chellemi, D. O. (2020). Are substrate-mediated microbial community shifts the future of soilborne disease management? Acta Hortic. 1270, 83–95. doi: 10.17660/ActaHortic.2020.1270.9

CrossRef Full Text | Google Scholar

Subbarao, K. V., Kabir, Z., Martin, F. N., and Koike, S. T. (2007). Management of soil-borne diseases in strawberry using vegetable rotations. Plant Dis. 91, 964–972. doi: 10.1094/PDIS-91-8-0964

PubMed Abstract | CrossRef Full Text | Google Scholar

Šumane, S., Kunda, I., Knickel, K., Strauss, A., Tisenkopfs, T, des Ios Rios, I., et al. (2018). Local and farmers' knowledge matters! How integrating informal and formal knowledge enhances sustainable and resilient agriculture. J. Rural Stud. 59. 232–241. doi: 10.1016/j.jrurstud.2017.01.020

CrossRef Full Text | Google Scholar

Teixeira, P., Colaianni, N. R., Fitzpatrick, C. R., and Dangl, J. L. (2019). Beyond pathogens: microbiota interactions with the plant immune system. Curr. Opin. Microbiol. 49, 7–17. doi: 10.1016/j.mib.2019.08.003

PubMed Abstract | CrossRef Full Text | Google Scholar

The Agricultural European Innovation Partnership (EIP-AGRI) Focus Group (2015). IPM Practices for Soil-Borne Diseases: Final Report. October (2015). (Brussels, Belgium: European Commission), 48. Available online at: https://ec.europa.eu/eip/agriculture/en/publications/eip-agri-focus-group-soil-borne-diseases-final (accessed on March 11, 2022).

Google Scholar

Thomas, H., Legard, D., and Rowe, D. (2014). “A review of the final three seasons (2012, 2013 and 2014) of research and grower demonstrations of the raised bed trough (RaBeT) substrate production system,” in California Strawberry Commission Annual Production Research Report 2014-2015. (Watsonville, CA) 117–139.

Google Scholar

Thomashow, L. S., LeTourneau, M. K., Kwak, Y. S., and Weller, D. M. (2019). The soil-borne legacy in the age of the holobiont. Microb. Biotechnol. 12, 51–54. doi: 10.1111/1751-7915.13325

PubMed Abstract | CrossRef Full Text | Google Scholar

Toju, H., Peay, K. G., Yamamichi, M., Narisawa, K., Hiruma, K., Naito, K., et al. (2018). Core microbiomes for sustainable agroecosystems. Nature Plants 4, 247–257. doi: 10.1038/s41477-018-0139-4

PubMed Abstract | CrossRef Full Text | Google Scholar

Trivedi, P., Delgado-Baquerizo, M., Trivedi, C., Hamonts, K., Anderson, I. C., and Singh, B. K. (2017). Keystone microbial taxa regulate the invasion of a fungal pathogen in agro-ecosystems. Soil Biol. Biochem. 111, 10–14. doi: 10.1016/j.soilbio.2017.03.013

CrossRef Full Text | Google Scholar

USDA-NRCS (2021). Healthy Soil for Life. Available onlline at: https://www.nrcs.usda.gov/wps/portal/nrcs/detailfull/national/soils/health/?cid=nrcs142p2_053846 (accessed December 19, 2021)

Google Scholar

van Bruggen, A. H. C., and Finckh, M. R. (2016). “Plant diseases and management approaches in organic farming systems,” in Annual Review of Phytopathology, Vol. 54, eds J. E. Leach, and S. Lindow, (San Mateo, CA), 25–54. doi: 10.1146/annurev-phyto-080615-100123

PubMed Abstract | CrossRef Full Text | Google Scholar

van Bruggen, A. H. C., Goss, E. M., Havelaar, A., van Diepeningen, A. D., Finckh, M. R., and Morris, J. G. (2019). One Health - cycling of diverse microbial communities as a connecting force for soil, plant, animal, human and ecosystem health. Sci. Total Environ. 664, 927–937. doi: 10.1016/j.scitotenv.2019.02.091

PubMed Abstract | CrossRef Full Text | Google Scholar

van Bruggen, A. H. C., and Semenov, A. M. (2000). In search of biological indicators for soil health and disease suppression. Agric. Ecosyst. Environ. Appl. Soil Ecol. 15, 13–24. doi: 10.1016/S0929-1393(00)00068-8

CrossRef Full Text | Google Scholar

vanEngelsdorp, D., Evans, J. D., Saegerman, C., Mullin, C., Haubruge, E., Nguyen, B. K., et al. (2009). Colony collapse disorder: a descriptive study. PLoS ONE 4, e6481. doi: 10.1371/journal.pone.0006481

PubMed Abstract | CrossRef Full Text | Google Scholar

Wall, D.H., Bardgett, R.D., Behan-Pelletier, V.M., Herrick, J.E., Jones, T.H., Ritz, K. (Eds.), et al. (2012). Soil Ecology and Ecosystem Services. New York, NY: Oxford University Press. doi: 10.1093/acprof:oso/9780199575923.001.0001

CrossRef Full Text | Google Scholar

Wall, D. H., Nielsen, U. N., and Six, J. (2015). Soil biodiversity and human health. Nature 528, 69–76. doi: 10.1038/nature15744

PubMed Abstract | CrossRef Full Text | Google Scholar

Warner, K. (2007). Agroecology in Action: Extending Alternative Agriculture Through Social Networks. Cambridge, MA: MIT Press. doi: 10.7551/mitpress/1164.001.0001

CrossRef Full Text | Google Scholar

Wei, Z., Friman, V.-P., Pommier, T., Geisen, S., Jousset, A., and Shen, Q. (2020). Rhizosphere immunity: targeting the underground for sustainable plant health management. Front. Agr. Sci. Eng. 7, 317–328. doi: 10.15302/J-FASE-2020346

CrossRef Full Text | Google Scholar

Wezel, A., Herren, B. G., Kerr, R. B., Barrios, E., Gonçalves, A. L. R., and Sinclair, F. (2020). Agroecological principles and elements and their implications for transitioning to sustainable food systems. a review. Agron. Sustain. Dev. 40, 40. doi: 10.1007/s13593-020-00646-z

CrossRef Full Text | Google Scholar

Wick, A. F., Haley, J., Gasch, C., Wehlander, T., Briese, L., and Samson-Liebig, S. (2019). Network-based approaches for soil health research and extension programming in North Dakota, USA. Soil Use Manage. 35, 177–184. doi: 10.1111/sum.12444

CrossRef Full Text | Google Scholar

Wilhelm, S., Storken, R. C., and Sagen, J. E. (1961). Verticillium wilt of strawberry controlled by fumigation of soil with chloropicrin and chloropicrin-methyl bromide mixtures. Phytopathology 51, 744–748.

Google Scholar

Wolf, M. (2015). Is there really such a thing as “One Health”? Thinking about a more than human world from the perspective of cultural anthropology. Soc. Sci. Med. 129, 5–11. doi: 10.1016/j.socscimed.2014.06.018

PubMed Abstract | CrossRef Full Text | Google Scholar

Worrall, S. (2017). Without Bugs, we Might all be Dead. Book Talk. National Geographic. Available online at: https://www.nationalgeographic.com/pages/topic/book-talk (accessed December 19, 2021)

Google Scholar

Xu, Y., Goodhue, R. E., Chalfant, J. A., Miller, T., and Fennimore, S. A. (2017). Economic viability of steam as an alternative to preplant soil fumigation in California Strawberry Production. HortScience 52, 401–407. doi: 10.21273/HORTSCI11486-16

CrossRef Full Text | Google Scholar

Zavatta, M., Muramoto, J., Mazzola, M., and Shennan, C. (2021). Rotation length, crop rotation, anaerobic soil disinfestation and mustard seed meal affect organic strawberry yield and soil-borne disease incidence in California. Acta Hort. 1309, 501–508. doi: 10.17660/ActaHortic.2021.1309.72

CrossRef Full Text | Google Scholar

Keywords: soil health assessment, soil-borne disease management, integrated pest management, non-fumigant alternatives, soil suppressiveness, agroecology, soil-plant-microbe interactions, organic farming

Citation: Muramoto J, Parr DM, Perez J and Wong DG (2022) Integrated Soil Health Management for Plant Health and One Health: Lessons From Histories of Soil-borne Disease Management in California Strawberries and Arthropod Pest Management. Front. Sustain. Food Syst. 6:839648. doi: 10.3389/fsufs.2022.839648

Received: 20 December 2021; Accepted: 03 March 2022;
Published: 28 March 2022.

Edited by:

Jesus Fernandez Bayo, University of California, Davis, United States

Reviewed by:

Timothy Bowles, University of California, Berkeley, United States
Qiuxia Wang, The Scripps Research Institute, United States

Copyright © 2022 Muramoto, Parr, Perez and Wong. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Joji Muramoto, am9qaSYjeDAwMDQwO3Vjc2MuZWR1

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