Opinion: Response to questions about common mycorrhizal networks

Common mycorrhizal networks (CMNs) are networks of mycorrhizal fungal hyphae held in common by at least two plants (Horton 2015;Rillig et al. 2024) and were first discovered in the laboratory by Reid & Woods (1969) and later supported by Finlay & Read (1986) and Perry et al. (1989). Simard et al. (1997) contributed to this knowledge by investigating underground transmission of carbon between ectomycorrhizal paper birch and Douglas-fir as well as arbuscular mycorrhizal western redcedar trees in the mixed temperate rainforests of western Canada. This body of pioneering work was followed by decades of creative peer-reviewed research by many scientists investigating the structure and function of CMNs in various forests around the world (see reviews including Newman (1988); Simard et al. (2012); Horton (2015); Tedersoo et al. (2020); Klein et al. (2023), and others). Research on the role of CMNs in the regenerative nature of forest ecosystems has recently come under targeted criticism by Karst et al. (2023), Henriksson et al. (2023), and Robinson, DG et al. (2023). These criticism articles question the veracity and interpretations of the peer reviewed research. They were triggered by the memoir of Simard (2021), who told of how her experiences shaped her research, and what she thinks her findings about CMNs mean for forests in Canada. An important aspect of our roles as scientists is to ensure clarity of our research to support future informed thought and investigations. In the following paragraphs, we address some of the questions and perceptions about CMNs raised by these authors.A brief review of the four main questions scientifically investigated about CMNs in forests provide context for our response to the criticisms. Notably, the three criticism articles generally dismiss evidence for all four questions. The first question, whether CMNs exist in forest ecosystems, has been investigated over the past five decades using increasingly sophisticated tools, from microscopy to DNA sequencing, microsatellites, and isotopic tracing. These studies, in our view, have revealed that CMNs can connect the roots of trees with other trees (see Figure 1; Beiler et al. 2010), as well as with compatible seedlings, shrubs, or mycoheterotrophic herbs (Selosse et al. 2006;Tedersoo et al. 2020;Authier et al. 2022;Merckx et al. 2024). The second question investigated has been whether CMNs facilitate nutrient, carbon, water or infochemical transfer among trees. This has also been demonstrated, and most studies show multiple belowground pathways functioning simultaneously, including CMNs, mycorrhizal roots, and soil (Simard et al. 1997;Babikova et al. 2013;Horton 2015;Klein et al. 2016). The third question, how resource transfer between trees varies in forests, has been investigated using field and associated greenhouse and lab studies. These studies have demonstrated that transfer is affected by a range of factors in forests, including the light, water, nutrient and health status of donor and recipient trees (Simard et al. 1997;Teste et al. 2010;Song et al. 2015;Klein et al. 2016), and the characteristics of the fungal species in the CMN (Teste et al. 2009, Merckx et al. 2024). A fourth question, whether membership in the CMN affects performance of trees, has also been investigated and results reveal this is also context dependent, as would be expected in complex systems like forests (Levin 2005). Nevertheless, evidence exists that linking into CMNs in forests can affect establishment of seedlings (Booth & Hoeksema 2008;Teste et al. 2009;Bingham & Simard 2011), growth or carbon status of mature trees (Klein et al. 2016;Birch et al. 2020), and performance of mycoheterotrophic plants (Selosse et al. 2006).This body of research investigating the structure and function of CMNs has fundamentally shifted how scientists understand forests (Perry et al. 2008), not only as collections of individual trees and plants competing for resources (Nylund 2016), but as connected systems of multiple complex interactions (Simard et al. 2012;Beiler et al. 2015). Whenever there is such a fundamental shift in knowledge, however, there is resistance (Rowell 2017), and the three critiques by Karst et al. (2023), Henriksson et al. (2023), andRobinson, DG et al. (2023) generally conclude this body of research is inadequate to inform our understanding of forests. In the following paragraphs, we address the main points raised by these authors, with more detailed responses to select statements in Table 1.In the first paper, Karst et al. (2023) provide negative commentary against public media interpretations of the memoir of Simard (2021) to open their case that there is a positive citation bias regarding the role of CMNs in forests. They argue there is insufficient evidence that CMNs contribute to regeneration processes in forests. There are several weaknesses in their analysis as follows. First, their search of CMN research in the primary literature (Reporting Summary, https://www.nature.com/articles/s41559-023-01986-1#additional-information) is obtuse, narrow and incomplete. As detailed in Table 1, they rely on subjective evaluations to determine which 18 studies to choose for their analysis, and then use elusive criteria to determine whether these papers have a positive bias. For example, they choose to exclude all studies investigating nurse tree facilitation of seedling establishment because they argue CMN effects cannot be disentangled from mycorrhizal colonization benefits (Table 1). However, scholars have argued facilitation of seedling establishment is likely the most important function of CMNs in natural ecosystems (Perry et al. 1989;Nara 2006;Horton et al. 2015;Rillig et al. 2023). For each of the 18 selected papers, Karst et al. (2023) automatically counted the number of years in the paper's publication record, which augmented their sample size to 273 and increased the power of their tests. The rationale for this enhancement of sample size was vague and lacked evidence that each year was represented by a citation bias in the literature. In their analysis, they also failed to adjust their methods to account for the inherent growth of sample size over time as researchers increase numbers of investigations in an emergent field. Regardless, whether there is any citation bias in the literature, this does not override the fact that studies show all tree species are mycorrhizal dependent and CMN-dependent facilitation and transfer have been demonstrated (Klein et al. 2023;Rillig et al. 2024). It is unfortunate these key points were overlooked in the review process. Karst et al. (2023) further imply that CMN-related field studies discount the role of alternative belowground resource transfer pathways to CMNs, such as through the soil or disconnected networks. Karst's criticism is echoed by Robinson DG et al. (2023) and Henriksson et al. (2023). However, as shown repeatedly by Simard et al. (1997Simard et al. ( , 2012)), and verified by others as detailed above, belowground transfer among trees occurs through multiple belowground transfer pathways simultaneously. All of these studies discussed alternative explanations to CMNs, contrary to the criticisms they did not. Regardless of this, Simard et al. (1997) found that a fraction (18%) of carbon isotope was transmitted to arbuscular mycorrhizal western redcedar compared with that between ectomycorrhizal paper birch and Douglas-fir, providing experimental evidence for carbon transfer through the CMN and simultaneously and to a lesser degree through the soil. Here, all three species had comparably vigorous and overlapping mycorrhizal roots, as naturally occurred in the surrounding forest (Simard et al. 1997;Twieg at al. 2008), rendering results that were realistic of the natural system. If, as Karst et al (2023) imply, transfer patterns in Simard et al. (1997) could be accounted for by differing root densities, and hence the gathering power of the different species, logic dictates that arbuscular mycorrhizal cedar growing among the two ectomycorrhizal trees would gather only one-fifth of the soil resources going to the ectomycorrhizal trees. Given the comparable health and vigor of the cedar roots and shoots to the other species of seedlings in the study, however, this is highly unlikely. Moreover, Karst's implication that the existence of one pathway rules out another, when they claim that transfer via mycorrhizal fungi had not been shown here in the field, misses the complexity of forest ecosystems.The three criticism articles imply that the carbon transfer measured would be insignificant to plants because they say isotopes in these studies did not enter recipient shoots (Karst et al. 2023;Henriksson et al. 2023;Robinson et al. 2023). However, our studies have repeatedly demonstrated that significant amounts of carbon are transferred into both shoots and roots of recipient seedlings through CMNs and other pathways (e,g., Simard et al. 1997;Teste et al. 2009;Philip et al. 2010;Song et al. 2015). In keeping with these findings, Klein et al. (2016) and Cahanovitc et al. (2022) have also found transfer into shoots of trees. This type of transfer has been associated with establishment of seedlings and mycoheterotrophic plants, which scientists argue are among the most important roles of CMNs in forests (see above; van der Heijden & Horton 2009;Rillig et al. 2024;Merckx et al. 2024). Moreover, the requirement of transfer into shoots assumes that carbon supply is the limiting factor in the photosynthetic process, and dismisses the likelihood that carbon subsidies to roots and associated mycorrhizae enhance the gathering of soil nutrients essential for photosynthesis. Perry & Oetter (2024) found that growth of Douglas-fir in low light was limited by magnesium, not carbon supply, indicating the essential role of mycorrhizas in productivity. As with other issues, the critics are not looking at the bigger picture. Karst et al. (2023) further argued that our research ignores the important role of competition in forest dynamics, possibly because CMN research in general has generated interpretations regarding cooperative relationships from trading of resources or infochemicals. However, none of our articles negate the process of competition in forests. Instead, we repeatedly discuss that multiple types of species interactions occur simultaneously, including competition, and that understanding forest dynamics must account for this complexity (Perry et al. 1989;Simard et al. 1997Simard et al. , 2012;;Simard & Vyse 2006). This complexity is readily evident in the mature, multicohort, multi-storied temperate forests where these experiments were conducted, where seedlings readily establish in the understory of old trees following small scale natural disturbances (Figure 1). In younger plantation forests absent of old trees and where competition may be less intense, CMNs may play a lesser role in forest dynamics. Nevertheless, many of our experiments tracing resource transfer between trees through belowground pathways have been conducted in recently planted forests (e.g., Simard 1997;Teste et al. 2009), and we have also successfully mapped the architecture of CMNs in young Douglas-fir forests (van Dorp et al. 2020), suggesting CMNs also exist in young temperate forests, albeit with lower complexity and more regular typology.Our discovery of kin recognition in trees has also been discounted by Karst et al. (2023) because the precise belowground mechanism by which trees recognize their genetic relatives remains elusive (Gorzelak et al. 2015;Pickles et al. 2017;Asay et al. 2020). This dismissal is short-sighted because the novel discovery could, for example, lead to a greater diversity of reforestation practices in western Canada, which currently relies heavily on clearcutting with artificial regeneration (Simard & Vyse, 1996). By providing support for natural regenerative processes as an alternative or supplement to even-aged plantations, which are vulnerable to climate-related failures and wildfires (Clason et al. 2022), this finding could help in a transition towards more resilient regeneration methods, such as use of overstory retention (Franklin et al. 2018, Simard et al. 2020). In a large-scale experiment crossing a 900-km climate gradient in interior Douglas-fir forests (Simard et al. 2020;Roach et al. 2021), for example, Simard et al. (2021) and Harris et al. (2024) have found that increasing levels of overstory retention facilitate regeneration success in increasingly arid regional climates. Henriksson et al. (2023) mistakenly compare our work in interior Douglas-fir forests of Canada to boreal pine forests in Europe, which have not been part of our research. The individual papers we have published provide results applicable to the temperate forests where the studies occurred (e.g., Simard et al. 1997;Teste et al. 2009;Beiler et al. 2010;Bingham & Simard 2011). It is well known that different species in specific ecosystems behave differently, and studies in the boreal pine forests of Scandinavia (Henriksson et al. may not that CMNs play the role as in et al. 2015). in boreal forests, for example, open in temperate forests of Canada naturally in the and CMNs of trees. results are and context dependent, and the or of a in one forest does not negate et al. the as Henriksson et al. (2023), Karst et al. (2023) and Robinson et al. DG (2023) our peer reviewed articles on belowground carbon transfer in temperate forests of Canada to forests in the This is we have not such statements in the literature. The evidence is however, that mycorrhizas play a role in the nature of interactions among trees. For example, of temperate and forest there is positive among in ectomycorrhizal forests, but negative in arbuscular mycorrhizal forests et al. et al. et al. 2023). These that mycorrhizal colonization by et al. et al. or CMNs et al. et al. may play a role in these forest is to the role of CMNs in different forest and It is important to in understanding these which could be important in to climate et al. Robinson, DG et al. (2023) to tree and claim that is to forests of However, they have the of the tree in (2021) memoir for to the public about the regenerative nature of interior Douglas-fir forests in Canada. Robinson, DG et al. (2023) also to to support their but only of Henriksson et al. (2023) and Karst et al. (2023). Robinson, DG et al. (2023) further two different types of CMN carbon and nutrient transfer to our which is on in Douglas-fir forests of Canada. These two types of mycorrhizal fungi are with and et al. et al. 2024). Karst et al. (2023) a of that must be any research on CMNs be in forests, but these are to in the field the and nature of forests (Klein et al. et al. 2024). is not that lab or greenhouse experiments with this is for any of complex natural and does not mean any relationships in complex systems such as forests must the of their and a of to their It is the of research to alternative explanations that have a greater from the published However, Karst et al. (2023) they provide that peer reviewed research. A more to and but this does not research investigating the role of CMNs in forest ecosystems et al. the (Simard was in the public can whether forest on & is the of our are through the of and that and CMNs are part of these processes (Perry et al. 1989;Simard et al. 2012;Beiler et al. et al. The of Simard (2021) was to in how CMNs help temperate forests, and whether the of these and relationships through forest is the of and climate et al. et al. et al. or whether more are et al. et al. et al. such as were to help these more to the tree have been in for & 2021), as well as in western literature (e.g., the use of in the for the of & Moreover, many have practices that their understanding of relationships in forests, including of trees or trees et al. et al. et al. 2022), and these could inform practices as climate et al. we argue that our peer-reviewed literature on CMNs against the targeted criticisms of Karst et al. (2023), Henriksson et al. (2023), DG et al. (2023), which to then peer-reviewed that our articles discount the role of alternative transfer pathways to CMNs, negate the of competition in forests, did not carbon transfer to or that we our findings to all forests, are not These criticism articles to provide any experimental evidence that would discount the peer reviewed literature. In our view, our research has contributed to a shift in how we forests and this may be important for more for and forests in our Karst et al. (2023), et al. (2023), and Robinson et al. can be from on media to their as various of media we three common CMNs are in resources are transferred through CMNs, in increased tree seedling and mature trees resources and to through media and the literature have and The is to the public in knowledge, but is not media is by Karst et al. as part of the including CMN colonization of plants can be as evidence (Karst et al. The claim there is limited evidence that CMNs are in forests, in of their research that CMN existence (e.g., et al. et al. and Hoeksema They exclude all research where CMNs between plants and seedlings they these studies cannot CMN effects from fungal colonization of seedlings is one of the most important of the Karst et al. conclude that the roots of trees and seedlings and many mycorrhizal fungi are fungal be also that of hyphae and mycorrhizal root occurs to and and use this as an against the of evidence for the body of research on nurse plants or trees ignores the role that CMNs of plants play in is by many scholars to be the most important function of CMNs in forests (e.g., Perry et al. 1989;Nara 2006). As Beiler et studies were conducted in Douglas-fir forests to understory seedling dynamics the CMNs of old trees. and are well known processes in CMNs and not negate the evidence found in peer-reviewed research that CMNs studies experiments using or are to provide evidence for CMNs (Karst et al. The argue there is insufficient evidence from studies, or from experiments using isotopic or any to establish that CMNs exist or facilitate of resources from one to However, they that conducted at can provide evidence for a linking the roots of different trees in They roots are by the species of mycorrhizal suggesting that fungal be are multiple of evidence for the existence of CMNs, including from studies using microsatellites, as well as from DNA sequencing, microscopy and isotope studies using or natural mycorrhizal type These studies have been conducted in temperate and ecosystems, and have been in several including Simard et al. ( In our research, we have a range of in interior Douglas-fir ecosystems, including isotope tracing (Simard et al. et al. et al. and Simard et al. et al. Dorp et al. et 2009), DNA (e.g., et al. and that experimental has and of these peer reviewed studies evidence that trees in interior forests are in a and that these relationships among trees affect the scientists in this field use multiple when about CMNs in their there are four studies of of CMNs by Beiler et al. et al. ( , et al. ( and and Dorp et al. in interior Douglas-fir forests of Canada, and one in the in pine forests of et al. 2006). et al. also carbon transmission is associated with in interior Douglas-fir Research is (Karst et al. The argue that there tree species any on the existence of CMNs in forests we a of these tree species and is and this literature is growing around the It would be to a of species and forests, and this field is However, detailed studies that CMNs in forests is and time and not The fact that these studies are time to however, does not the peer review research that has been As not generally that is an of which publication of this research multiple field not in growth or as evidence for CMNs in forests (Karst et al. The their literature search to field experiments because they say are most to on forest and because the role that trees play in forests can only be in the (Karst et al. Karst et al. (2023) not the of field with greenhouse experiments and laboratory analysis to the role of CMNs in forests. and field with greenhouse growth analysis to understand of in patterns (e.g., et By experiments and analysis, Karst et al. (2023) have limited their to evidence for the existence and functioning of CMNs in are several of the of including studies in CMN research in forests. For example, Klein et al. (2016) isotope tracing in the lab to mature trees in the field. to carbon from old growth trees to seedlings et al. the of trees in the field by first nurse trees in the then growing younger to forest CMNs are the only pathway for resource transmission between trees that can be in forests (Karst et al. The argue that CMNs are for resource transfer and that other transfer pathways are peer reviewed studies belowground resource transmission among trees have found the existence for multiple belowground transfer not (see review by Horton et al. 2015). In our we discuss evidence for multiple pathways (e.g., Simard et al. laboratory results to the field, providing evidence for both and carbon transfer between species, for the of as well as soil and for of transfer in field belowground pathways for transmission of carbon, and water have also been in the studies reviewed in Simard et al. et al. ( , have shown that the and pathway of belowground resource transfer varies on the water and status of the trees, as well as the and of the CMN interpretations are a from (Karst et al. The results from this et al. have been as evidence that CMNs resources a that was a from (Karst et al. work there is a of types in forests, including competition and and that resource between to affect these Simard et al. (1997) our results the of carbon transfer in natural then the of one species on cannot be a understanding of carbon transfer through mycorrhizal fungi and soil A more of carbon among plants as a of transfer may have for of and for and (Simard et al. critics on competition in forests, as is in forest and support the of plantations, of and enhancement of of and other work that a diversity of types occurs in forests (e.g., Simard & Vyse The to a CMN has on or growth (Karst et al. The conclude there are forest experiments that that the to a CMN affects growth or their including and Hoeksema and et al. (2021), the who that and the in of Douglas-fir trees with numbers of evidence for facilitation of establishment exists in temperate and ecosystems, where ectomycorrhizal seedlings to establish around trees or et al. & Simard et al. et al. in interior Douglas-fir forests are by into the CMN that exists among the trees less by in the have found that seedlings that not by CMNs not et al. CMN effects on seedling and growth in Douglas-fir forests have shown greater effects on where they had to mycorrhizal root and soil This was when seedlings from planted as were to of mature trees, or were growing in or more arid (Teste & 2008;Teste et 2009;Bingham & 2011). There is evidence trees with through CMNs (Karst et al. The there is evidence that trees resources or of to through recognition of or has been well in plants and found to via roots and mycorrhizas ( et al. et al. as well as 2015). have to this literature with evidence for kin recognition in interior Douglas-fir, and with studies that is by roots and mycorrhizas et al.

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