Resource allocation in tragedy of the commons game in plants for belowground competition

Highlights

• Tragedy of the commons occur when plants compete for limited resources.

• Growth dynamics and resource allocation was applied to belowground competition in plants.

• We found evolutionarily stable resource allocation strategy in the presence of neighboring plant.

• Root overproliferation did not always occur in the tragedy of the commons game.

• Careful observation required for examining plant species in game theoretic situation.

Abstract

The tragedy of the commons (TOC) has been well known since it was proposed and has been widely applied not only to human society but also to many taxa. An increasing number of studies have focused on TOC in belowground competition in plants. In the presence of neighbors, plants overproduce roots to acquire more nutrients than their competitors, resulting in a reduction in reproductive yield. Game-theoretic studies on TOC in plants usually consider the amount of root biomass as a strategy and do not consider the growth of plants. However, root volume is considered an outcome of the decision-making of plants on whether they allocate more resources to the root. In this study, we incorporated resource allocation and growth dynamics into the TOC game in plants and explored the evolutionarily stable resource allocation strategy in the presence of neighbors. We demonstrated that TOC generally occurs when fitness per individual is always reduced because of the competitive response. However, the overproliferation of roots, which is emphasized as an indicator of TOC, did not necessarily occur, or was sometimes difficult to detect when fitness is largely or completely determined by root biomass. This result suggests the importance of careful observation for examining whether plant species engage in a TOC game

Introduction

The tragedy of the commons (TOC) is a situation in which a shared resource is overused or depleted due to the conflict between individuals and collective rationality (Hardin, 1968). This concept has been adopted not only in human society but also to explain similar situations for other organisms, such as viruses, bacteria, animals, and even plants (Rankin et al., 2007). In the last two decades, an increasing number of studies have reported TOC in plant competitions (Gersani et al., 2001). Because plants are limited by soil nutrient availability in many terrestrial ecosystems, many studies have reported competitive response and TOC in belowground competition for nutrients (Gersani et al., 2001). It has also been applied largely to the competition of plants for light (Schieving and Poorter, 1999, Falster and Westoby, 2003) and water (Zhang et al., 1999).

TOC in belowground competition is observed as an overproduction of roots, resulting in a decrease in seed production, when plants share soil (Gersani et al., 2001, Maina et al., 2002, O'Brien et al., 2005, O’Brien and Brown, 2008). Several studies have introduced an evolutionary game-theoretical perspective on competition in plants (McNickle and Dybzinski, 2013). The amount of roots produced is usually defined as a strategy, and an evolutionarily stable amount of root is derived (Gersani et al., 2001, O’Brien and Brown, 2008; McNickle et al., 2012; McNickle and Brown, 2014, Cabal et al., 2020). However, TOC in belowground competition in plants is not always observed (Semchenko et al., 2007, Lankinen, 2008, Markham and Halwas, 2011). In such a case, these plant species are presumed not to be capable of detecting competitors, and the amount of roots is thought to be determined only by the amount of available nutrients in the soil, resulting in an ideal free distribution of root volume (McNickle and Brown, 2014).

In previous theoretical studies that considered the TOC in belowground competition, the amount of roots was usually defined as a strategy, and a fixed amount of root was assumed to exist in the soil from the beginning of cultivation (Gersani et al., 2001, McNickle and Brown, 2014). However, the amount of roots is considered an outcome of growth rather than the strategy. The consideration of plant growth or its dynamics has been an essential aspect in the evolution of life-history strategies. Plants are thought to achieve maximum fitness yield by controlling the growth schedule (Cohen, 1971, Iwasa and Cohen, 1989) and optimize their life cycle through growth dynamics (Guilbaud et al., 2015). The root production of a plant is generally regulated by genes (Schmid et al., 2013), physiological responses (Meier et al., 2013), and resource allocation levels (Bhatt et al., 2011). Plants can change resource allocation to the growth of roots and shoots under given environmental conditions (Yang and Midmore, 2005, Schultz et al., 2013). A more plausible strategy is the resource allocation rate (Aikio and Markkola, 2002). Therefore, exploring resource allocation strategies and evaluating reproductive yield and the amount of produced roots because of competition should be extremely reasonable for studying TOC in plants.

In this study, we incorporated resource allocation to plant growth into a game-theoretical model for belowground competition in plants. We considered two essential resources for plant growth, light, and nutrients (Aikio and Markkola, 2002). Light and nutrient availability are proportional to aboveground and belowground biomass, respectively; hence, optimal resource allocation rates exist for both resources. In presence of a neighbor, the amount of nutrients absorbed was determined by the ratio of the amount of one's roots to the total amount of roots of the two plants’ roots, which was a game situation. We demonstrate that there exists an evolutionarily stable allocation of resources in the presence of a neighboring plant. The TOC generally occurs when fitness per individual is always reduced under competition. However, fitness was decreased without root overproliferation when fitness was strongly correlated with root biomass, indicating that overproliferation of roots is not necessarily observed in belowground TOC games in plants. The difference in root production between the solitary and competition plants was sometimes considerably small, indicating that the detection of TOC was difficult, and competition experiments would likely lead to different interpretations of the results.