Forum
Commentary Challenging cherished ideas in mycorrhizal ecology: the Baylis postulate The Baylis postulate has been an influential idea in arbuscular mycorrhizal (AM) research (Baylis, 1975; Fitter, 2004). The original formulation of the postulate made the prediction that only plants with elaborate root systems could grow in the absence of mycorrhiza (Baylis, 1975). A generalized form of the Baylis postulate stated that the root architectural parameters of the plant host could represent a good predictor of its mycorrhizal growth response (MGR), defined as the percentage difference in biomass of AM-inoculated vs non-AM-inoculated plants grown under identical conditions. The generalized formulation of the Baylis postulate has been widely used in AM research, although it has never been explicitly tested (e.g. Fitter, 2004). In this issue of New Phytologist, Maherali (pp. 191–199) describes the results of a metaanalysis to assess the empirical support for this hypothesis. Maherali demonstrated that, despite having included studies in which the relationship between root architectural parameters and MGR was significant, the overall effect was neutral. This result was robust to the exclusion of individual studies in a sensitivity analysis.
‘Building on past data collections, we are now in the middle of a period of data synthesis – exciting times for mycorrhizal ecology.’
Ecological meta-analysis and AM research Maherali quantitatively tested a long-held belief in the mycorrhizal research community through a synthesis approach, and found an overall null result. A non-significant result following a technically sound meta-analytical approach can be as useful as finding significant effects. Ecological meta-analysis has progressed considerably over the last few years. In the past, many meta-analytical attempts in ecology have struggled with the peculiarities of ecological data, such as common deviation of ecological variables from normality and poor data reporting practices in the original papers (Gurevitch & Hedges, 1999). The nature of ecological experiments additionally implies that multiple experiments are commonly reported in the same study, resulting in issues of Ó 2014 The Authors New Phytologist Ó 2014 New Phytologist Trust
non-independence. Non-independence can also arise from shared phylogenetic history across the organisms tested. A number of dedicated studies on ecological meta-analysis (e.g. Lajeunesse, 2011; Hillebrand & Gurevitch, 2014) have recently paved the way for effectively addressing these issues. Using meta-analytical techniques, it may be feasible to address many of the cherished stories in mycorrhizal research which, despite having been of a general interest, require massive amounts of data to be convincingly tested and have thus never been appropriately addressed (Table 1). The extended form of the Baylis postulate that is tackled in Maherali is a great example. The meta-analyst has to make do with the experimental design of the original studies. Meta-analytical studies are thus subject to a number of shortcomings which, although they still need to be acknowledged, do not detract from the high value of producing a quantitative summary of the existing literature. The present study of Maherali is no exception. Primarily, these relate to the small number of published studies that meet the inclusion criteria; indeed, it was alarming to realize how little work has been carried out with regard to comparative assays of the relationship between root architecture and MGR. Moreover, a rarely appreciated fact in meta-analyses is that the method yields quantitative effect size estimates that are representative of average experimental conditions. In Maherali, such an average experimental condition represented in the meta-analysis might have been an intermediate to low fertility growth substrate. MGR is a metric that is strongly dependent on the growth conditions experienced by the plant. It is unclear whether a stronger relationship could have been detected for soils with even lower fertility (the subset of studies that were included in the meta-analysis and were carried out under conditions of extreme nutrient limitation); indeed, the significant result that was retrieved for many of the individual studies, when analyzed independently, suggested that some unmeasured parameters, perhaps including soil fertility, exert a strong effect on the relationship. Many of the shortcomings of the use of MGR as the response variable are acknowledged in Maherali. To these we would like to add that the metric assumes that biomass is a proxy for fitness, that the artificial experimental conditions are representative of field conditions and that the AM fungal isolate used in each experiment associates with all plant hosts with the same efficiency. Finally, it is important to note that the extended Baylis postulate overlooks AM fungi-related contributions to the plant host other than nutrient assimilation. These caveats aside, the result reported in the study have interesting implications.
Independence between mycorrhizal dependence and root architecture: implications Why could the message of the analysis of Maherali be important for plant and AM ecology? Primarily because this result suggests that New Phytologist (2014) 204: 1–3 1 www.newphytologist.com
2 Forum
New Phytologist
Commentary
Table 1 Some examples of beliefs in mycorrhizal ecology that either have not been tested or for which existing evidence is based on a few individual studies: these example hypotheses could benefit from a quantitative analysis through meta-analytical techniques Hypotheses
Comments
Plants that associate with ectomycorrhizal fungi exhibit stronger mycorrhizal growth response (MGR) than those that associate with arbuscular mycorrhizal (AM) fungi
Although there have been several tests on plants that associatewith both groups of fungi, the results have never been quantitatively synthesized
The trade balance model hypothesis
According to this hypothesis, discussed extensively by Johnson (2010 – it was formulated by her in the mid-1990s), the importance of AM associations increases whenever there is an asymmetry in the relative availability of nitrogen (N) and phosphorus (P)
The importance of mycorrhiza for plant invasions differs between Europe and America
The hypothesis was proposed by Pringle et al. (2009). In their report, the authors make a call for more rigorous support for the hypothesis
The effect of AM fungi on plant diversity is dependent on the mycorrhizal status of the dominant species in a plant community
The hypothesis originates from Bergelson & Crawley (1988). There have been multiple studies that have yielded support for this hypothesis, but no quantitative synthesis exists
Legumes exhibit, on average, stronger MGR than non-N-fixing plants
N fixation in legumes implies stronger P requirements of the plant that could be met through association with AM fungi. Yet, several plants in the Fabaceae family, such as members of the genus Lupinus, are only weakly mycorrhizal (Wang & Qiu, 2006; Brundrett, 2009). This hypothesis and the fact that C4 grasses are believed to be more mycorrhizal dependent than C3 grasses represent two popular hypotheses that link MGR and plant functional type
even plants with a highly branched root system may respond strongly to their AM associates. One possibility is that plants with highly branched root systems profit from their AM fungal community by receiving different services (e.g. pathogen protection – Fitter, 2005). The performance of these different functions may require trade-offs in growth investments for the Glomeromycotan fungus (Fitter, 2005). In this case, it remains to be seen whether the AM fungal communities that associate with plants with highly branched root systems are distinct from those that associate with plants with less branched roots. By adopting a phytocentric point of view, the implications for the plant host could be quite dramatic. Root architecture, together with the functional type to which the plant host belongs (e.g. legumes, C3 grasses), have traditionally been considered to be the best predictors of MGR. If MGR cannot be consistently linked to root architecture, the outcome of the symbiosis should be considerably more idiosyncratic than originally thought. In mycorrhizal ecology, difficulties associated with the quantification of other mycorrhizal functions have led to the literature being heavily biased towards the quantification of nutritional components of the symbiosis (Veresoglou & Rillig, 2013). What is known is that, under specific conditions, the symbiosis can result in reduced plant host growth (Johnson, 2010) and that common experimental practices (e.g. use of soil diluted with sand; pot experiments that induce strong nutrient limitation) tend to exaggerate mycorrhizal nutritional effects. Although MGR should not be confused with AM dependence, it may represent a convenient proxy. If existing predictors of MGR perform badly, what could determine biomass-related responses of the symbiosis for individual plant species? One idea is that the overall fitness benefits plants receive from the symbiosis could be stochastic, reflecting a dynamic ‘negotiation’ procedure within an iterative biological market (Selosse & Rousset, 2011). A positive MGR New Phytologist (2014) 204: 1–3 www.newphytologist.com
(assuming that MGR is assayed in a manner that encompasses AMrelated effects on plant survival) could reflect a successive negotiation in evolutionary time of a response that fluctuates around an ambient average level (that might well approximate neutrality – Veresoglou & Halley, 2012). In such a case, it is unlikely that some plant species could secure disproportionately high AM symbiosis-related benefits. Perhaps, not surprisingly, the loss of the mycorrhizal condition in AM plants has occurred independently multiple times across the plant phylogeny (Wang & Qiu, 2006).
Conclusion The study of Maherali has addressed an important gap in the mycorrhizal literature. Despite a number of uncertainties, there are a range of exciting opportunities for further research that emanate from this study. These include the evaluation of the extent to which environmental conditions drive the MGR–root architecture relationship and the assessment of whether AM fungal communities of plants with highly branched root systems functionally resemble those of plants with coarser roots. Building on past data collections, we are now in the middle of a period of data synthesis – exciting times for mycorrhizal ecology.
Acknowledgements We thank Ian Dickie and Hafiz Maherali for valuable comments. Stavros D. Veresoglou1,2* and Matthias C. Rillig1,2 1
Freie Universit€at Berlin, Institut f€ ur Biologie, Altensteinstr. 6, D-14195 Berlin, Germany; Ó 2014 The Authors New Phytologist Ó 2014 New Phytologist Trust
New Phytologist 2
Commentary
Berlin-Brandenburg Institute of Advanced Biodiversity Research (BBIB), D-14195 Berlin, Germany (*Author for correspondence: tel +49 (0)30 838 53172; email [email protected])
References Baylis GTS. 1975. The magnolioid mycorrhiza and mycotrophy in root systems derived from it. In: Sanders FE, Mosse B, Tinker PB, eds. Endomycorrhizas. London, UK: Academic Press, 373–389. Bergelson JM, Crawley JM. 1988. Mycorrhizal infection and plant species diversity. Nature 334: 202. Brundrett MC. 2009. Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant and Soil 320: 37–77. Fitter AH. 2004. Magnolioid roots – hairs, architecture and mycorrhizal dependency. New Phytologist 164: 15–16. Fitter AH. 2005. Darkness visible: reflections on underground ecology. Journal of Ecology 93: 231–243. Gurevitch J, Hedges LV. 1999. Statistical issues in ecological meta-analyses. Ecology 80: 1142–1149.
Forum 3
Hillebrand H, Gurevitch J. 2014. Meta-analysis results are unlikely to be biased by differences in variance and replication between ecological lab and field studies. Oikos 123: 794–799. Johnson NC. 2010. Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales. New Phytologist 185: 631–647. Lajeunesse MJ. 2011. On the meta-analysis of response ratios for studies with correlated and multi-group designs. Ecology 92: 2049–2055. Maherali H. 2014. Is there an association between root architecture and mycorrhizal growth response? New Phytologist 204: 191–199. Pringle A, Bever JD, Gardes M, Parrent JL, Rillig MC, Klironomos JN. 2009. Mycorrhizal symbioses and plant invasions. Annual Review of Ecology, Evolution, and Systematics 40: 699–715. Selosse MA, Rousset F. 2011. The plant–fungal marketplace. Science 333: 828–829. Veresoglou SD, Halley JM. 2012. A model that explains diversity patterns of arbuscular mycorrhizas. Ecological Modelling 231: 146–152. Veresoglou SD, Rillig MC. 2013. Accounting for the adaptation deficit of non-mycorrhizal plants in experiments. Plant and Soil 366: 33–34. Wang B, Qiu YL. 2006. Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16: 299–363. Key words: Baylis’ postulate, meta-analysis, mycorrhizal ecology, mycorrhizal growth response, synthesis studies.
www.newphytologist.com
[email protected]
[email protected]
www.newphytologist.com
Ó 2014 The Authors New Phytologist Ó 2014 New Phytologist Trust
New Phytologist (2014) 204: 1–3 www.newphytologist.com
Commentary Challenging cherished ideas in mycorrhizal ecology: the Baylis postulate The Baylis postulate has been an influential idea in arbuscular mycorrhizal (AM) research (Baylis, 1975; Fitter, 2004). The original formulation of the postulate made the prediction that only plants with elaborate root systems could grow in the absence of mycorrhiza (Baylis, 1975). A generalized form of the Baylis postulate stated that the root architectural parameters of the plant host could represent a good predictor of its mycorrhizal growth response (MGR), defined as the percentage difference in biomass of AM-inoculated vs non-AM-inoculated plants grown under identical conditions. The generalized formulation of the Baylis postulate has been widely used in AM research, although it has never been explicitly tested (e.g. Fitter, 2004). In this issue of New Phytologist, Maherali (pp. 191–199) describes the results of a metaanalysis to assess the empirical support for this hypothesis. Maherali demonstrated that, despite having included studies in which the relationship between root architectural parameters and MGR was significant, the overall effect was neutral. This result was robust to the exclusion of individual studies in a sensitivity analysis.
‘Building on past data collections, we are now in the middle of a period of data synthesis – exciting times for mycorrhizal ecology.’
Ecological meta-analysis and AM research Maherali quantitatively tested a long-held belief in the mycorrhizal research community through a synthesis approach, and found an overall null result. A non-significant result following a technically sound meta-analytical approach can be as useful as finding significant effects. Ecological meta-analysis has progressed considerably over the last few years. In the past, many meta-analytical attempts in ecology have struggled with the peculiarities of ecological data, such as common deviation of ecological variables from normality and poor data reporting practices in the original papers (Gurevitch & Hedges, 1999). The nature of ecological experiments additionally implies that multiple experiments are commonly reported in the same study, resulting in issues of Ó 2014 The Authors New Phytologist Ó 2014 New Phytologist Trust
non-independence. Non-independence can also arise from shared phylogenetic history across the organisms tested. A number of dedicated studies on ecological meta-analysis (e.g. Lajeunesse, 2011; Hillebrand & Gurevitch, 2014) have recently paved the way for effectively addressing these issues. Using meta-analytical techniques, it may be feasible to address many of the cherished stories in mycorrhizal research which, despite having been of a general interest, require massive amounts of data to be convincingly tested and have thus never been appropriately addressed (Table 1). The extended form of the Baylis postulate that is tackled in Maherali is a great example. The meta-analyst has to make do with the experimental design of the original studies. Meta-analytical studies are thus subject to a number of shortcomings which, although they still need to be acknowledged, do not detract from the high value of producing a quantitative summary of the existing literature. The present study of Maherali is no exception. Primarily, these relate to the small number of published studies that meet the inclusion criteria; indeed, it was alarming to realize how little work has been carried out with regard to comparative assays of the relationship between root architecture and MGR. Moreover, a rarely appreciated fact in meta-analyses is that the method yields quantitative effect size estimates that are representative of average experimental conditions. In Maherali, such an average experimental condition represented in the meta-analysis might have been an intermediate to low fertility growth substrate. MGR is a metric that is strongly dependent on the growth conditions experienced by the plant. It is unclear whether a stronger relationship could have been detected for soils with even lower fertility (the subset of studies that were included in the meta-analysis and were carried out under conditions of extreme nutrient limitation); indeed, the significant result that was retrieved for many of the individual studies, when analyzed independently, suggested that some unmeasured parameters, perhaps including soil fertility, exert a strong effect on the relationship. Many of the shortcomings of the use of MGR as the response variable are acknowledged in Maherali. To these we would like to add that the metric assumes that biomass is a proxy for fitness, that the artificial experimental conditions are representative of field conditions and that the AM fungal isolate used in each experiment associates with all plant hosts with the same efficiency. Finally, it is important to note that the extended Baylis postulate overlooks AM fungi-related contributions to the plant host other than nutrient assimilation. These caveats aside, the result reported in the study have interesting implications.
Independence between mycorrhizal dependence and root architecture: implications Why could the message of the analysis of Maherali be important for plant and AM ecology? Primarily because this result suggests that New Phytologist (2014) 204: 1–3 1 www.newphytologist.com
2 Forum
New Phytologist
Commentary
Table 1 Some examples of beliefs in mycorrhizal ecology that either have not been tested or for which existing evidence is based on a few individual studies: these example hypotheses could benefit from a quantitative analysis through meta-analytical techniques Hypotheses
Comments
Plants that associate with ectomycorrhizal fungi exhibit stronger mycorrhizal growth response (MGR) than those that associate with arbuscular mycorrhizal (AM) fungi
Although there have been several tests on plants that associatewith both groups of fungi, the results have never been quantitatively synthesized
The trade balance model hypothesis
According to this hypothesis, discussed extensively by Johnson (2010 – it was formulated by her in the mid-1990s), the importance of AM associations increases whenever there is an asymmetry in the relative availability of nitrogen (N) and phosphorus (P)
The importance of mycorrhiza for plant invasions differs between Europe and America
The hypothesis was proposed by Pringle et al. (2009). In their report, the authors make a call for more rigorous support for the hypothesis
The effect of AM fungi on plant diversity is dependent on the mycorrhizal status of the dominant species in a plant community
The hypothesis originates from Bergelson & Crawley (1988). There have been multiple studies that have yielded support for this hypothesis, but no quantitative synthesis exists
Legumes exhibit, on average, stronger MGR than non-N-fixing plants
N fixation in legumes implies stronger P requirements of the plant that could be met through association with AM fungi. Yet, several plants in the Fabaceae family, such as members of the genus Lupinus, are only weakly mycorrhizal (Wang & Qiu, 2006; Brundrett, 2009). This hypothesis and the fact that C4 grasses are believed to be more mycorrhizal dependent than C3 grasses represent two popular hypotheses that link MGR and plant functional type
even plants with a highly branched root system may respond strongly to their AM associates. One possibility is that plants with highly branched root systems profit from their AM fungal community by receiving different services (e.g. pathogen protection – Fitter, 2005). The performance of these different functions may require trade-offs in growth investments for the Glomeromycotan fungus (Fitter, 2005). In this case, it remains to be seen whether the AM fungal communities that associate with plants with highly branched root systems are distinct from those that associate with plants with less branched roots. By adopting a phytocentric point of view, the implications for the plant host could be quite dramatic. Root architecture, together with the functional type to which the plant host belongs (e.g. legumes, C3 grasses), have traditionally been considered to be the best predictors of MGR. If MGR cannot be consistently linked to root architecture, the outcome of the symbiosis should be considerably more idiosyncratic than originally thought. In mycorrhizal ecology, difficulties associated with the quantification of other mycorrhizal functions have led to the literature being heavily biased towards the quantification of nutritional components of the symbiosis (Veresoglou & Rillig, 2013). What is known is that, under specific conditions, the symbiosis can result in reduced plant host growth (Johnson, 2010) and that common experimental practices (e.g. use of soil diluted with sand; pot experiments that induce strong nutrient limitation) tend to exaggerate mycorrhizal nutritional effects. Although MGR should not be confused with AM dependence, it may represent a convenient proxy. If existing predictors of MGR perform badly, what could determine biomass-related responses of the symbiosis for individual plant species? One idea is that the overall fitness benefits plants receive from the symbiosis could be stochastic, reflecting a dynamic ‘negotiation’ procedure within an iterative biological market (Selosse & Rousset, 2011). A positive MGR New Phytologist (2014) 204: 1–3 www.newphytologist.com
(assuming that MGR is assayed in a manner that encompasses AMrelated effects on plant survival) could reflect a successive negotiation in evolutionary time of a response that fluctuates around an ambient average level (that might well approximate neutrality – Veresoglou & Halley, 2012). In such a case, it is unlikely that some plant species could secure disproportionately high AM symbiosis-related benefits. Perhaps, not surprisingly, the loss of the mycorrhizal condition in AM plants has occurred independently multiple times across the plant phylogeny (Wang & Qiu, 2006).
Conclusion The study of Maherali has addressed an important gap in the mycorrhizal literature. Despite a number of uncertainties, there are a range of exciting opportunities for further research that emanate from this study. These include the evaluation of the extent to which environmental conditions drive the MGR–root architecture relationship and the assessment of whether AM fungal communities of plants with highly branched root systems functionally resemble those of plants with coarser roots. Building on past data collections, we are now in the middle of a period of data synthesis – exciting times for mycorrhizal ecology.
Acknowledgements We thank Ian Dickie and Hafiz Maherali for valuable comments. Stavros D. Veresoglou1,2* and Matthias C. Rillig1,2 1
Freie Universit€at Berlin, Institut f€ ur Biologie, Altensteinstr. 6, D-14195 Berlin, Germany; Ó 2014 The Authors New Phytologist Ó 2014 New Phytologist Trust
New Phytologist 2
Commentary
Berlin-Brandenburg Institute of Advanced Biodiversity Research (BBIB), D-14195 Berlin, Germany (*Author for correspondence: tel +49 (0)30 838 53172; email [email protected])
References Baylis GTS. 1975. The magnolioid mycorrhiza and mycotrophy in root systems derived from it. In: Sanders FE, Mosse B, Tinker PB, eds. Endomycorrhizas. London, UK: Academic Press, 373–389. Bergelson JM, Crawley JM. 1988. Mycorrhizal infection and plant species diversity. Nature 334: 202. Brundrett MC. 2009. Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant and Soil 320: 37–77. Fitter AH. 2004. Magnolioid roots – hairs, architecture and mycorrhizal dependency. New Phytologist 164: 15–16. Fitter AH. 2005. Darkness visible: reflections on underground ecology. Journal of Ecology 93: 231–243. Gurevitch J, Hedges LV. 1999. Statistical issues in ecological meta-analyses. Ecology 80: 1142–1149.
Forum 3
Hillebrand H, Gurevitch J. 2014. Meta-analysis results are unlikely to be biased by differences in variance and replication between ecological lab and field studies. Oikos 123: 794–799. Johnson NC. 2010. Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales. New Phytologist 185: 631–647. Lajeunesse MJ. 2011. On the meta-analysis of response ratios for studies with correlated and multi-group designs. Ecology 92: 2049–2055. Maherali H. 2014. Is there an association between root architecture and mycorrhizal growth response? New Phytologist 204: 191–199. Pringle A, Bever JD, Gardes M, Parrent JL, Rillig MC, Klironomos JN. 2009. Mycorrhizal symbioses and plant invasions. Annual Review of Ecology, Evolution, and Systematics 40: 699–715. Selosse MA, Rousset F. 2011. The plant–fungal marketplace. Science 333: 828–829. Veresoglou SD, Halley JM. 2012. A model that explains diversity patterns of arbuscular mycorrhizas. Ecological Modelling 231: 146–152. Veresoglou SD, Rillig MC. 2013. Accounting for the adaptation deficit of non-mycorrhizal plants in experiments. Plant and Soil 366: 33–34. Wang B, Qiu YL. 2006. Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16: 299–363. Key words: Baylis’ postulate, meta-analysis, mycorrhizal ecology, mycorrhizal growth response, synthesis studies.
www.newphytologist.com
[email protected]
[email protected]
www.newphytologist.com
Ó 2014 The Authors New Phytologist Ó 2014 New Phytologist Trust
New Phytologist (2014) 204: 1–3 www.newphytologist.com
