Management Implications
Nonnative trees are abundant across agricultural landscapes in northern Florida and southern Georgia. Removal of these trees is costly, and they have no commercial use once they have been cut down. Growing mushrooms on nonnative trees has several potential benefits. Selling mushrooms produced on nonnative trees can provide an additional source of on-farm income for small-scale producers through the production of edible mushrooms. The production of mushrooms on weedy tree species would help defray the cost of their removal and conserve native oak (Quercus L.) trees that are the traditional log substrate for shiitake mushroom production. Mushroom fungus also speeds the decomposition of logs, which otherwise may occupy productive land or require removal. The ability of weedy trees to provide a substrate for mushroom production may provide landowners with an additional incentive to remove invasive trees and increase the removal rates of these trees.
Introduction
Because trees are large and long-lived organisms, an invasive tree can alter the structure and function of its surrounding ecosystem more readily than smaller or more ephemeral species (van Wilgen and Richardson Reference van Wilgen and Richardson2014). As a result of their impacts, nonnative trees are now recognized as some of the worst invasive species worldwide (van Wilgen and Richardson Reference van Wilgen and Richardson2014). There are 163 species of trees and woody shrubs considered invasive in North America (Richardson and Rejmánek Reference Richardson and Rejmánek2011). In Florida, at least 13 tree species are listed as noxious (Florida State. 5B 57.001 and 5B-57.007, last ammended Septermber 2020) and/or considered invasive by the state (UF/IFAS/CAIP 2023). Many counties in Florida, such as Palm Beach and Miami-Dade, require landowners to remove invasive trees during development or redevelopment of land (Miami-Dade County 2023; Palm Beach County 2023).
Removal of invasive trees is time-consuming and expensive. Between 2009 and 2014, state and federal agencies spent US$45 million annually to control invasive plants on state conservation land in Florida (Hiatt et al. Reference Hiatt, Serbesoff-King, Lieurance, Gordon and Flory2019). During this time, the two most costly terrestrial weeds to control were trees: paperbark tree [Melaleuca quinquenervia (Cav.) S.F. Blake] and Brazilian peppertree (Schinus terebinthifolia Raddi) (Hiatt et al. Reference Hiatt, Serbesoff-King, Lieurance, Gordon and Flory2019). From 1998 to 2004, the Florida Department of Environmental Protection spent almost US$0.75 million treating Chinese tallowtree [Triadica sebifera (L.) Small] on 1,619 hectares (4,000 acres) of natural areas in north and central Florida (McCormick Reference McCormick2005). Currently, T. sebifera infests nearly 202,343 hectares (0.5 million acres) of forests, wet prairies, and ruderal areas in California, southern Texas, along the Gulf Coast to Florida, and the southern Atlantic coast states north to North Carolina (EddMapS 2023). Even for a private landowner or small farmer, the cost of cutting down invasive trees and removing the waste generated by branches and trunks is time-consuming and costly, negatively impacting farm sustainability.
Most mushrooms produced in the United States are Agaricus species, including white button, cremini, and portobello (Agaricus bisporus) (USDA-NASS 2022). Non-Agaricus mushrooms, including shiitake mushrooms (Lentinula edodes) and oyster mushrooms (Pleurotus ostreatus var. florida), are considered specialty mushrooms (USDA-NASS 2022). Shiitake mushrooms are a white-rot, Agaricales fungus that utilizes dead wood of broad-leaved trees for growth and reproduction. Shiitake mushrooms are used in culinary dishes, are broadly considered to be medicinal, and are used in traditional medicine (Ahmad et al. Reference Ahmad, Arif, Mimi, Zhang, Ding and Lyu2023). Oyster mushrooms, another saprotrophic white-rot Agaricales, is a highly sought after culinary mushroom and is a fungus commonly used for mycoremediation (Rhodes Reference Rhodes2014). Cultivation of gourmet edible and medicinal mushrooms has gained popularity throughout the southeastern United States (Stamets Reference Stamets2000) and across the country generally (Morgan Reference Morgan2023). Commercial production of specialty mushrooms (oyster, shiitake, and others) grew 12.5% from 2020 to 2022 (USDA-NASS 2022). Prices of specialty mushrooms also rose during this period, resulting in a 32% increase in the value of specialty mushrooms to US$87.4 million (USDA-NASS 2022). Many small farmers have begun cultivating mushrooms using logs from native tree species as a substrate for mushroom mycelium. Production of mushrooms on hardwood logs (versus on a sawdust substrate) produces high-value mushrooms that can be sold to restaurants or directly to consumers at farmer’s markets (Kimmons et al. Reference Kimmons, Phillips and Brauer2003). The average wholesale price per pound of shiitake mushrooms in 2022 was US$3.51, and oyster mushrooms had a wholesale price of US$3.04, compared with US$1.67 for portobello mushrooms and US$0.71 for white button mushrooms (Agaricus spp.) (USDA-NASS 2022). Retail prices for fresh, log-grown shiitake mushrooms range from US$26.46 to US$44.09 per kilogram (US$12.00 to US$20.00 per pound) (Frey Reference Frey2020), and in some markets up to US$52.91 per Kg (US$24.00 per pound) for shiitakes and between US$26.46 and US$52.91 per Kg (US$12.00 and US$24.00 per pound) for oyster mushrooms (B Moyers, extension program specialist, personal communication). In one state extension report, sales of log-grown shiitake mushrooms were estimated to reach US$96.2 million in 2017 (Gabriel Reference Gabriel2022), representing a significant demand for log-grown mushrooms.
While much is known about cultivating mushrooms on native oak (Quercus L.) species, there is a lack of information about use of alternative substrates, including lower-value native species as well as nonnative trees. Two native trees, sweetgum (Liquidambar styraciflua L.) and red maple (Acer rubrum L.), and the invasive species tree-of-heaven [Ailanthus altissima (Mill.) Swingle], have all been tested for suitability as shiitake mushroom substrate as alternatives to white oak (Quercus alba L.) (Frey et al. Reference Frey, Durmus, Sills, Isik and Comer2020). Liquidambar styraciflua was the most suitable alternative to Q. alba, with A. rubrum less suitable, and A. altissima not suitable for mushroom production (Frey et al. Reference Frey, Durmus, Sills, Isik and Comer2020). O’Donnell et al. (Reference O’Donnell, Moulton and Stack2019) inoculated the invasive tree glossy privet (Ligustrum lucidum W.T. Aiton) with turkey tail fungi (Trametes versicolor) to aid decomposition of felled logs. Logs from L. lucidum supported production of this fungus, which has traditional medicinal uses, and the fungus aided in breaking down the logs, reducing the fire hazard in natural areas (O’Donnell et al. Reference O’Donnell, Moulton and Stack2019). Previous research showed that standing wood from the invasive A. altissima supported mycelial growth of oyster mushrooms and chicken-of-the-woods (Laetiporus sulphureus) (Baran Reference Baran2010). The abovementioned research demonstrated that mushrooms can be grown on an unconventional log substrate, such as an invasive tree species, resulting in financial return, sustainable benefits, and management of a nonnative invasive species (Baran Reference Baran2010; Frey et al. Reference Frey, Durmus, Sills, Isik and Comer2020; O’Donnell et al. Reference O’Donnell, Moulton and Stack2019). Such an outcome may increase motivation for land managers, homeowners, and small-scale farmers to reduce invasive species by cutting down nonnative trees on their land for mushroom cultivation. Furthermore, if edible fungi perform well on nonnative species, mushroom cultivators may be convinced to utilize wood from invasive trees that would otherwise be discarded, thus making efficient use of an un-utilized on-farm resource.
We evaluated the potential of using logs of nonnative trees common to the southeastern United States to produce edible and marketable mushrooms, turning unsustainable nonnative tree species into a sustainable, small-farm commodity. Five invasive species were evaluated in this study, and their ability to produce edible mushrooms was compared against results from logs of Quercus spp., which are the trees commonly used for mushroom production in southeastern United States.
This 2-yr study addressed two objectives: (1) to determine whether invasive tree species that are common in the southeastern United States produce edible shiitake and oyster mushrooms; and, if so, (2) how do the mushroom yields on the invasive species compare with the Quercus spp. standards. We chose four metrics to evaluate mushroom production: the proportion of logs that fruited, the total weight of mushrooms produced by log, the number of mushrooms produced by log, and the weight per mushroom.
Materials and Methods
Mushroom Production Study Locations
Logs of each tree species were harvested, inoculated, and stored at four cooperating small farms: Full Earth Farm, Gadsden County, FL; Little Eden Heirloom Farm, Wakulla County, FL; Sanguon’s Organic, Decatur County, GA; and Artzi Organic Farm, Thomas County, GA. All cooperating small farms were located in the Atlantic Plain with a humid, subtropical climate with an average temperature of 20.0 C and 120 cm of precipitation annually. Logs were harvested, inoculated, and stored at each of the four farms using the process described in the following section. Logs were inoculated with fungal mycelium in the first year of the study and mushrooms were harvested twice, in 2015 and 2016, while mushrooms were harvested from logs inoculated in the second year only once, in 2016.
Log Preparation and Inoculation Process
Log Preparation
Trees were cut in February to March when the sapwood was rich in sugars and before foliation. Cut stumps of invasive species were treated with triclopyr (Garlon 3A®, Dow AgroSciences, Indianapolis, IN) immediately after cutting to kill roots and prevent sprouting (Enloe et al. Reference Enloe, Loewenstein and Cain2019). The trunks were cut into 0.90-m-long logs of 10- to 20-cm diameter. Once logs were felled, they were kept away from the soil to avoid contamination with saprophytic fungi and handled in a manner to not damage the bark layer (Stamets and Chilton Reference Stamets and Chilton1983). Logs were stacked on pallets, kept close to the ground, and shaded for 2 to 3 wk before inoculation. This “resting” period was included to allow for the possibility that antifungal properties of the wood needed to dissipate (Stamets Reference Stamets2005).
Inoculation
Inoculation procedures were conducted on-site at cooperating farms. Before inoculation, the log surface was lightly cleaned with a wire brush to remove soil, algae, lichens, and insect eggs. Holes were drilled in logs for the introduction of mushroom mycelium using angle grinders equipped with specialized 8.5-mm-diameter screw-tip drill bits, which were attached to the grinder spindle using a specialized adaptor (Field and Forest Products, Peshtigo, WI). These bits had an integrated stop that allowed holes to be drilled to the depth that exactly accommodated spawn plugs made from birch dowels inoculated with mycelia. Evenly spaced holes (0.80-cm diameter by 2.54-cm deep) were power drilled into each log 10 cm apart, arranged longitudinally down the log axis in a diamond pattern (Stamets Reference Stamets2000). Immediately after drilling, spawn plugs were driven into holes using rubber mallets. Holes were then sealed with heated soy wax using small wooden paint brushes to conserve moisture and prevent infection by competing organisms. The cut ends of the logs were also sealed with wax.
Commercial catalogues of mycelium spawn producers/sellers generally suggest 45 to 50 spawn plugs per 0.90 m by 15 cm (length by diameter) log (Field and Forest Products 2017; Fungi Perfecti 2017). Our inoculation rate was based on the surface area of this “standard log”: (S = 2πrh = 0.42 m2), where S is the surface area, r is the log radius, and h is the log height. Therefore, assuming a 15-cm-diameter log received 50 plugs, each 2.54-cm change in log diameter correlated to an increase (or decrease) of eight plugs. The number of plugs per log was determined, the information recorded, and each log marked with an aluminum tag containing a unique number, tree species, and randomly selected fungus treatment (shiitake or oyster mushroom).
Incubation
Inoculated logs were stacked on pallets under shade cloth (70% shade factor) (Green-Tek, Clinton, WI) for 7 mo to allow the spawn to fully colonize the logs. Logs were watered as needed using a sprinkler system during the summer incubation period to support mycelium growth. Supplemental watering in this humid southern climate was required only once per week during weeks without any rainfall.
Production
In October, approximately 8 mo after inoculation, when mycelium growth in the logs was visible in the cut faces, logs were removed from the pallet stacks and soaked in a tank of water for 24 h (Frey Reference Frey2020). Logs were then propped along a wire fence in an “A-frame” manner. The fence included a short wooden platform to keep the log bases away from the soil. Logs were spaced to allow access to all surfaces for mushroom harvesting. Mushroom primordia started forming within 2 wk of initiation. Mushrooms formed throughout the log surface, not only in the spawn-plugged holes. Logs were watered as needed with sprinkling systems to maintain moisture and soaked in water tanks every 6 wk to stimulate mushroom production.
Inoculation Study
For the inoculation study trees were provided by collaborators from across the state of Florida. An initial assessment study was conducted in 2014 to evaluate the ability of two common fungi species to successfully inoculate logs from five invasive tree species and produce edible mushrooms. Two native oak species, water oak (Quercus nigra L.) and laurel oak (Quercus laurifolia Michx.), commonly used by small-farm shiitake cultivators in the southeastern United States, were included as control treatments. The two Quercus spp. were lumped together as the control, as they were both common in woodlots and could not be adequately distinguished when harvested before leaf flush. Logs were inoculated with one of two shiitake varieties, Wide Range (WR) 46TM or Snow CapTM and a native Florida strain of oyster mushroom, P. ostreatus var. florida (Field and Forest Products). This oyster mushroom is a preferred variety for southern climates, because it fruits at warmer temperatures (Stamets Reference Stamets2000). The five nonnative tree species tested were Triadica sebifera, Chinaberry (Melia azedarach L.), silktree (Albizia julibrissin Durazz.), earleaf acacia (Acacia auriculiformis A. Cunn. ex Benth.), and M. quinquenervia. Acacia auriculiformis logs were harvested near the University of Florida/IFAS Indian River Research and Education Center in Ft. Pierce, FL, while M. quinquenervia trees were cut near Ft. Lauderdale, FL. Melia azedarach and A. julibrissin were harvested from Full Earth Farm in Gadsden County, FL.
Mushroom Production Study
Trees used for mycelium substrate in the production study were identified from woodlots, fencerows, and waste areas at cooperating farms. Based on results from the inoculation study, the inoculation and storage techniques were found to be appropriate, as mycelium growth was observed on all treated logs. Because data collected from the inoculation study identified poor production of oyster mushrooms from all tree species tested, a second strain of shiitake (Snow CapTM) was substituted for the oyster variety, and the production study was focused on the best-producing invasive tree species, T. sebifera, and the Quercus spp. control. The production study followed the same methods utilized for the inoculation study. Each cooperating farm received 20 to 42 logs of T. sebifera and 20 to 40 logs of Quercus spp.
Data Analysis
Mushrooms were harvested by hand on a weekly basis when fruiting occurred before spores had dropped from mushroom gills. Harvests were counted and weighed, and records were kept for production of each log. Logs were grouped by cohort according to inoculation and harvest year, so that mushrooms from logs inoculated and harvested in 2015 were assigned to cohort 1, mushrooms harvested in 2016 from the 2015 logs were cohort 2, and those harvested in cohort 3 were from logs inoculated and harvested in 2016. One farm, Sanguon’s Organic, recorded useful data on only a few occasions, so that farm was excluded from the analysis. A completely randomized design was used for each of the three farms with two levels of replication: multiple logs from each tree and multiple trees for each log species. For each inoculation year and harvest period, we used a chi-square test (PROC FREQ; SAS v. 9.4, SAS Institute, Cary, NC) to determine whether there was a difference in the proportion of fruiting logs. Non-fruiting logs are included in average yield and number of mushrooms calculations but excluded from mushroom size calculations.
To determine whether there were yield differences between Quercus spp. and T. sebifera logs, we used a generalized linear mixed model (PROC GLIMMIX; SAS v. 9.4) with a negative binomial distribution procedure on yield data (yield per log, number of mushrooms per log, and weight per mushroom). The fixed effects were tree species and harvest cohort, and the random effects were farm and individual tree. Mushroom yield data and weight per mushroom data were logarithmically transformed before analysis. Data for number of mushrooms were square-root transformed before analysis. Measures of central tendency are presented as untransformed means ± standard error of the mean (SEM).
Results and Discussion
Although mycelial growth was observed on all five species of trees during the inoculation study, only shiitake mushrooms fruited on the invasive trees. Both shiitake and oyster mushrooms fruited on the control. No shiitake mushrooms occurred on A. auriculiformis, M. azedarach, and A. julibrissin. Only a few shiitake mushrooms occurred on M. quinquenervia; thus, these data are not presented here. A substantial production of shiitake was gathered from both Quercus spp. and T. sebifera logs. Because oyster mushroom production was poor in the control and failed on all tested invasive trees, oyster mushrooms were excluded from the study (Table 1). The complete failure of oyster mushrooms in this study was believed to be a function of a decreased growth rate in the logs. We believe the oyster mushrooms would have fruited if given more time; however, this increased time to harvest would likely be detrimental to the profitability for producers.
Shiitake and oyster mushroom inoculation study on native and invasive tree species a
a A plus sign (+) indicates production of fruiting bodies from mushroom. Number of plus signs correlates to productivity of the tree species. A dash (—) indicates that no mushrooms were produced. Due to poor fruiting, results were not analyzed.
We compared shiitake mushroom yield (both weight in grams and number of mushrooms) and mushroom size (calculated as weight per mushroom) between Quercus spp. and T. sebifera logs for both inoculation years, resulting in three harvest cohorts. Data from the inoculation study were not statistically analyzed due to the poor performance of the mushrooms on the tree species besides Quercus spp. and T. sebifera (Table 1), and shiitake mushroom varieties were pooled for the production study.
Quercus spp. and T. sebifera logs were equally likely to fruit at Little Eden Heirloom Farm for all three cohorts of logs (Table 2). Quercus spp. logs were more likely to fruit at Artzi Organic Farm (χ2= 0.0016) and at Full Earth for two out of three cohorts (2015 χ2 = 0.0009 and 2016 χ2 = 0.028).
Proportion of fruiting logs by inoculation year and farm
Overall, Quercus spp. logs produced higher mushroom yields than T. sebifera logs. Quercus spp. logs produced 649.52 ± 37.24 g of mushrooms per log, and T. sebifera logs produced 265.45 ± 27.23 g of mushrooms per log (Table 3). There was a farm effect (F(2, 27.18) = 11.89, P = 0.002), a tree species effect (F(1, 36.58) = 8.48, P < 0.0061), and a cohort effect (F(2, 121.6) = 8.65, P = 0.0003). For this cohort, each Quercus spp. log on average produced 620.85 ± 75.56 g of mushrooms, while T. sebifera logs produced 166.13 ± 32.89 g. Quercus spp. and T. sebifera did not produce significantly different mushroom yields (grams per log) during the first year of the study (inoculated and harvested in 2015) (Quercus spp. = 751.92 ± 99.66; T. sebifera = 340.64 ± 64.32 g; Figure 1). Between Quercus spp. and T. sebifera logs that were inoculated and harvested in 2016, Quercus spp. logs had higher shiitake yields (624.95 ± 46.05 g) than the T. sebifera logs (273.50 ± 38.11 g).
GLM for effects of tree species, farm, and cohort on mushroom yield, mushroom number, and mushroom size a
a Mushroom yield and number of mushrooms included all logs. Only fruiting logs were used to calculate mushroom size.
Grams per log (mean ± SEM) of shiitake mushrooms produced on Quercus spp. or Triadica sebifera inoculated at two farms in year 1 (2015) and three farms in year 2 (2016) and harvested during the first harvest period (October 2015–March 2016) or the second harvest period (October 2016–March 2017). Within a species, different letters above bars indicate significant differences between treatments (P = 0.05).
Overall, Quercus spp. logs produced more mushrooms than T. sebifera logs over the 2 yr (F(1, 57.51) = 30.94, P = 0.0012). Individual Quercus spp. logs produced 33.18 ± 2.33 mushrooms annually, while T. sebifera logs produced 8.71 ± 0.93 mushrooms annually. This result was consistent over all inoculation and harvest days of the study (Figure 2). Mushroom size showed the reverse trend, with mushrooms produced on T. sebifera logs weighing more than Quercus spp.–produced mushrooms (F(1, 8.82) = 11.70, P = 0.0079). The average Quercus spp. –produced mushroom weighed 23.68 ± 0.80 g, while the average T. sebifera–produced mushroom weighed 36.30 ± 1.72 g (Figure 3). This difference was driven by the larger size of the T. sebifera mushrooms for a log’s first harvest in both 2015 and 2016.
Number of shiitake mushrooms (mean ± SEM) produced per Quercus spp. or Triadica sebifera log inoculated at two farms in year 1 (2015) and three farms in year 2 (2016) and harvested during the first harvest period (October 2015–March 2016) or the second harvest period (October 2016–March 2017). Within a species, different letters above bars indicate significant differences between treatments (P = 0.05).
Grams per mushroom (mean ± SEM) of shiitake mushrooms produced on Quercus spp. or Triadica sebifera logs inoculated at two farms in year 1 (2015) and three farms in year 2 (2016) and harvested during the first harvest period (October 2015–March 2016) or the second harvest period (October 2016–March 2017). Within a species, different letters above bars indicate significant differences between treatments (P = 0.05).
In this project, invasive trees were removed from farms and surrounding locations for use in mushroom production. We showed that T. sebifera, listed as a Florida Category 1 Invasive Species (“most invasive plant species”), produced edible shiitake mushrooms. Although the number of mushrooms was fewer on T. sebifera logs than on Quercus logs, the weight of individual mushrooms was greater on T. sebifera than Quercus for two out of three harvest cohorts. We also showed that four invasive tree species were deemed unsuitable for shiitake mushroom production—M. quinquenervia, A. auriculiformis, M. azedarach, and A. julibrissin. Conducting additional screening of other nonnative tree species for their ability to produce edible mushrooms has the potential to expand the production of edible mushrooms on weedy tree species. While M. quinquenervia, A. auriculiformis, M. azedarach, and A. julibrissin are all detrimental invasive plants in the southeastern United States, T. sebifera is considered the most damaging, because it is the most widespread. The ability to use this tree to produce individually larger, high-quality mushrooms is significant.
Log mushroom culture was developed in Asia more than 1,000 yr ago, and even today, thousands of small-scale shiitake growers use log culture to provide most mushrooms sold to markets (Stamets Reference Stamets2000). There continue to be many advantages of log mushroom culture. It is a simple and low-input method. As an alternative to burning nonnative invasive trees (which causes pollution, sudden emissions of carbon dioxide, and denitrification of soil), growing fungi on wood allows for the incorporation of nutrients back into the ecosystem, improvement in soil structure, and the gradual release of carbon dioxide. Fungi are the premier recyclers of organic waste, and they efficiently return nutrients to the ecosystem. Utilizing edible fungi to recycle invasive nonnative trees transforms a detrimental constituent on small farms into an income-producing natural resource.
A Google scholar search of the terms “bioaccumulation” and “shiitake mushroom” revealed no published accounts of negative effects to humans from eating mushrooms produced from plant species containing potentially toxic plant defensive compounds. In addition, the authors consumed many of the mushrooms produced on nonnative trees and experienced no negative effects. Finally, assumptions made about the non-toxicity of logs that served as mushroom-producing media included: (1) plant chemicals that serve as non-herbivore deterrents occurred primarily in the leaves and reproductive structures of the plants, not the wood; (2) if high levels of toxins were present in the wood, then they would interfere with the growth and survival of mycelium, preventing the formation of mushrooms (which was probably true for M. azedarach); and (3) commercially marketed edible mushrooms are safely produced on tree log species (i.e., black cherry [Prunus serotina Ehrh.]) that contain toxic chemicals without detrimental effects regarding human consumption. However, future studies may elucidate differences in chemicals derived from tissues of shiitake mushrooms when grown on different wood substrates.
Acknowledgments
The authors would like to thank the cooperating farmers at Full Earth Farm, Little Eden Heirloom Farm, Artzi Organic Farm, and Sanguon’s Organic for collecting mushroom harvest data. We also thank John Mass and Angela Galette for their technical assistance. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture. USDA is an equal opportunity provider and employer.
Funding statement
This research was funded by Southern SARE On Farm Research grant OS14-086.
Competing interests
The authors declare no competing interests.
