The ISME Journal (2017) 11, 2175–2180 © 2017 International Society for Microbial Ecology All rights reserved 1751-7362/17 www.nature.com/ismej PERSPECTIVE Applying allometric theory to fungi Carlos A Aguilar-Trigueros1,2, Matthias C Rillig1,2 and Thomas W Crowther3 1Institute of Biology, Freie Universität Berlin, Berlin, Germany; 2Berlin-Brandenburg Institute of Advanced Biodiversity Research, Berlin, Germany and 3Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands The ISME Journal (2017) 11, 2175–2180; doi:10.1038/ismej.2017.86; published online 14 July 2017 Introduction particularly to filamentous fungi. We do this by (i) outlining the conceptual basis behind allometric Fungi are prominent components of every ecosystem — theory; (ii) addressing the methodological challenges in terms of biomass, diversity and functioning. as well as implications of applying such theory to However, in contrast to many other taxonomic fungi; and (iii) characterizing the allometric scaling groups, we have a poor mechanistic understanding of fungal metabolic rate to body size as a prominent of the patterns in fungal community organization example in allometric scaling. While we focus on the and functioning. To address this gap, a growing scaling of metabolic rate to body size because of its number of researchers are beginning to characterize importance in predicting ecological relationships, fungal diversity in terms of traits that explain how we consider metabolic scaling as a springboard for fungi respond to and influence the environment that discussion that could lead to testing other (Crowther et al., 2014; Aguilar-Trigueros et al., scaling relationships in fungal biology in general. 2015). In this paper, we argue that body size is a trait that, although historically ignored in mycology, could be Definition of allometry and the scaling of a major axis for understanding the biology of fungi. metabolic rate Our argument is based on the fact that fungi vary considerably in size, ranging from single-celled In biology, allometry is traditionally understood as microscopic organisms to one of the largest living the scaling of trait variation to body size (Bonner, organisms on earth (Smith et al., 1992). Thus the 2011). This emphasis on body size relies on two scaling of fungal traits to body size or its proxies is main observations: First, living organisms vary in likely to capture a wealth of valuable baseline total body size during their ontogeny as well as information about the ecology and functioning of during their evolution, which has resulted in shifts those species. in body size within each kingdom. Second, there is a To support our argument, we draw on advances in strong correlation between body size and multiple plant and animal ecology that apply allometric relevant ecological and physiological traits. The theory (that is, scaling relationships between traits mechanisms behind these relationships to body and total body size) as a valuable conceptual frame- size depend on the trait, but they combine physical work. Allometric theory was originally used to and biochemical constraints (Peters, 1983) as well as understand developmental and evolutionary pat- adaptive evolution (Glazier, 2010). terns (Bonner, 2011), but it has since been used to In most cases, traits change disproportionally to explain ecological phenomena (for example, Brown body size. This is expressed as et al., 2004). Although allometric theory has been applied to Power function of body size: ecological phenomena, it has yet to be adopted in fungal biology. In this paper, we lay the foundations Y ¼ aM b ð1Þ of the approach and point out how this theory could be adapted to understand the causes and conse- or equivalently as: quences of size variation in the fungal kingdom, logY ¼ log a þ blog M; ð2Þ Correspondence: CA Aguilar-Trigueros, Institute of Biology, Freie Body size specific trait: Universitat Berlin, Altensteinstrasse 6, 14195 Berlin, Germany. E-mail: [email protected] Y À Received 19 December 2016; revised 15 April 2017; accepted ¼ aM b 1 25 April 2017; published online 14 July 2017 M Allometry in fungal ecology CA Aguilar-Trigueros et al 2176 or equivalently as: Fungi, a major group of eukaryotes, have not been considered in the development of metabolic theory Y of ecology, neither during its conception nor its later log ¼ log a þ ðÞb À 1 log M; ð3Þ B refinements over the last two decades (as Glazier (2010) points out). To address this important gap, in the next section, we develop a roadmap for applying allometric theory to fungi. where Y is the trait, M is the body size (usually in units of weight or volume), a is a coefficient of proportionality, and the power b is the scaling A roadmap for allometric scaling for fungi (allometric) factor (Niklas, 2004), which in many cases deviates from 1 (that is, disproportionality; see Defining fungal size Supplementary Figure S1 for representation of each Ideally, a measurement of size should capture the expression). Determining the value of this scaling total amount of matter and space that the body of an factor represents the core of allometric research, organism occupies at a particular point in time. In as it reflects the physiological and ecological allometric research, body size is usually measured as constraints to variation in body size in living biomass, either directly or—for convenience—using organisms (Glazier, 2010). Traits that have been different proxies for particular groups: biovolumes shown to scale allometrically to size in animals and or protein contents for unicellular organisms plants include growth rate, metabolic rate, strength, (Makarieva et al., 2005), or length measurements of life span, population density, competitive ability, body axes (for example, diameter, height) in plants and elemental incorporation rate, among others and animals (for example, Peters, 1983; Niklas, (Brown et al., 2004). Although many traits are likely 2004). Given that most fungi display indeterminate to scale with organismal size, we consider deter- growth, final body biomass can be methodologically mining metabolic scaling of fungi a first step in challenging to ascertain. This challenge may have introducing allometric research to fungal biology, contributed to the failure to incorporate allo- given its connections with many other performance metric theory into fungal ecology (and vice versa). characteristics. A promising approach is to use determinate growth Metabolic rate is expected to increase less propor- stages of fungi, such as sporocarp measurements tionally to body size based on geometric arguments: (biomass, height, diameter) in a way analogous to metabolic rate depends on the surface area available plants and animals (Pringle et al., 2015). However, to deliver nutrients and oxygen to each cell of an sporocarp formation (prevalent in a small group of organism's body, but surface area increases only fungal species), represents a very limited fungal correspond to a two-thirds increase in size. In life stage. contrast to this geometric expectation, empirical To address this shortcoming, we propose defining tests of metabolic scaling on diverse organisms fungal body size using measurements of vegetative commonly report higher scaling factors. There have mycelial colonies. Although the hyphae are the basic been numerous explanations for these deviations. units of filamentous fungi, we believe that a colony- For example, it has been proposed that as plant and level focus is useful because (i) the colony represents animals increase in size, they achieve higher surface the most prevalent fungal body state because soon area than expected for their size, resulting from their after an individual hypha forms, it branches profu- developing complex respiratory and circulatory sely, then anastomoses and finally coordinates systems (Bonner, 2011). growth and flow of nutrients to form complex tissue Further, the metabolic theory of ecology proposes (Moore et al., 2011); (ii) in many cases, fungal that as body size and metabolic rate account for the colonies can be distinguished from one another by amount of resources and energy an organism needs, observing them on the surface of substrates such as its scaling controls other ecological processes, from plant tissues, soil and litter layers, and wood, to the individual to the ecosystem level (Brown et al., name just a few. For example, colony biomass 2004). As initially formulated, this theory postulates accumulated after a given amount of time represents that the metabolic scaling to body size should follow the closest proxy of body size as it has been applied a common scaling factor of ¾. to other organisms (see Fuentes et al., 2015). In Recent reviews have challenged some of the tenets addition, we advocate scaling to other various of the metabolic theory of ecology. As more and measures of colony size such as ‘colony hyphal better data are collected from a greater diversity of length’, ‘colony extension rate’ or ‘hyphal branch- organisms, it has been shown that there is a large ing’, all of which represent valuable metrics to infer variation in scaling factors (for example, Makarieva the ecology of fungi. For example, colony hyphal et al., 2005; DeLong et al., 2010). It has also been length (analogous to total root length in plants) better pointed out that that metabolic rate may both affect represents the earlier stages of the fungal body, and and be affected by other biological and ecological might be more representative of the type of growth processes,