Plant Individuality: A Physiological Approach

1 Introduction

Individuality has been a hot topic for philosophers of biology for a considerable time.¹ Various conceptions of biological individuality have been proposed, and several of them have been seriously challenged by the specific characteristics of plants (Dupré 2010; Clarke 2012; Gerber 2018). We think that different domains of biology suggest different approaches to the problem of biological individuality, and highlight different aspects of the problem. In this paper, we consider what plant physiology can offer. We argue that it challenges how one might normally think of boundaries, pointing to them as vague, rather than distinct, while also indicating both vertical and horizontal coordination of physiological processes, which allows us to see coordinated systems at multiple scales. In this paper, we support this proposal with attention to the special attributes of plants.²

Philosophers have mostly approached plant individuality via conceptions of evolutionary individuality which focus on the unit of selection.³ Here we instead consider plants as physiological individuals. Since physiological individuality is about the unit of functioning, we believe it aligns well with the concept of the organism as a cohesive whole with differentiated parts that function in coordination (Mossio and Moreno 2010; Nuo de la Rosa 2010). We examine the extent to which plants can be seen as individual organisms, based on those physiological processes that enable them to coordinate their physical parts. Since we approach plant individuality through a focus on physiology and coordination, we also discuss plant parts and the practices through which these are individuated in plant science. Although we are not investigating plant cognition in this paper, we find it plausible that this coordination provides instances of plant cognition. Whereas in the case of animals much of this regulation and coordination is accomplished by the nervous system, in plants a similar function is served by the flow of hormones and other information-bearing molecules around the system. We think that plant physiological individuality often more or less coincides with plant cognitive individuality, as plants actively interact with their environments, perceive salient features of the environment, and coordinate their actions in ways appropriate to environmental conditions.⁴

To study plants as organisms with coordinated parts requires observing how they organise interactions between their parts at a particular developmental stage, as well as how this organisation projects the plant toward the organisation of later stages. The next part of the paper examines this coordination in plants and how it is regulated through source-sink balance in interaction with the environment. Source and sink concepts in plant science were first proposed by Mason and Maskell (1928), in their work on transport of carbohydrates in cotton plants (Chang and Zhu 2017). Source-sink balance, which is maintained via dynamic interactions between source and sink tissues, concerns the distribution of carbohydrates and minerals in a plant’s body. We argue that the coordination via source-sink balance (i.e., the physiological processes which enable this balance) can provide the basis for distinguishing the physiological individuality of a plant. We especially stress the importance of hormones in the maintenance of this stability. We will show how, depending on our research questions, we may think of plant physiological individuality as extending to wider limits in, for example, the cases of plant-plant interactions mediated by the microbiota, the growth of new ramets in a genet, and so on.

In the third part of the paper, we discuss the implications of this physiological perspective for the attribution of individuality to plants, arguing that while plants do often have a strong individuality, it is also often possible to divide plant processes into individuals in various non-overlapping ways. Finally, in the fourth part of the paper, we discuss this “promiscuous individualism” with specific reference to the processual nature of plants.

2 Coordination in Plants

Coordination, through the many physiological processes that maintain the source-sink balance, is a necessary capacity of plants. Although plants do not move like animals, they do move in several ways, including through their growth.⁵ Examples of growth processes that involve an adaptive response to the environment include the growth of branches towards areas which receive more light, the growth of roots towards a part of the soil with better composition or availability of nutrients, and the searching for support structures by vine tendrils. Other adaptive movements by plants include the timing of the opening and closing of stomata, regulated through a complex web of processes to optimise water content and carbon dioxide intake, and the movements of carnivorous plants to trap and digest their prey. A plant’s response to environmental cues, signals, and stressors is the outcome of internal signalling processes that enable plants to coordinate their bodies in ways appropriate to specific environments and maintain optimal source-sink balance regulation.⁶

3 Plants as Physiological Individuals

Plants are living systems, and as such, they are continuously self-organising through their interaction with the environment. This interaction constitutes a complex net of intertwined processes that extends into other plants and the environment. Although these extensions blur plants’ boundaries (for example through the arbuscular mycorrhiza-plant interaction), we can still frequently distinguish an individual plant as an individual organism, a dynamic entity actively changing its body and its environment through the behaviour that it produces in response to environmental cues. The organism as a whole, acts as one individual (a physiological individual).

Baedke (2019a) claims that both early twentieth century organism-centered biology and the recent revival of the centrality of the organism (Nicholson 2014) are challenged by perspectives that point to the lack of clear boundaries demarcating the organism. The entanglement of the organism with its environment does indeed challenge the attempt to delineate sharp boundaries for the former. Interactions between organism and environment, the latter including many other putative organisms, may directly or indirectly effect the metabolic pathways in various candidate organisms, or may even become parts of those pathways. This challenge is even more pressing for plants than animals, since in addition to having intimate interactions with microbiota, as do animals, they are also modular organisms¹⁴ that have semi-autonomous parts, can grow or reproduce in many different kinds of ways, and can become clones.

DiFrisco proposes that “physiological individuality is characterized by stable interaction gradients that are present when physiological interactions between parts are stronger or more frequent with each other than they are with parts of the environment” (DiFrisco 2018, 20). On the basis of source-sink balance regulations, we can often distinguish individual plants as physiological individuals on such a criterion. The coordination of plant parts (e.g., regulating source-sink balance) through interactions of many molecules and hormonal networks is stronger and more frequent than interactions with the environment. However, as discussed in the previous section in relation to plant-microbiota interactions involving chemical communication, we sometimes observe physiological individuality conceived in such a way as extending beyond the intuitively apparent physiological boundaries.

Another much-discussed case is the genet,¹⁵ which may consist of many individual-like ramets. A genet is a collection of modules or ramets developed from a single zygote (Clarke 2012) and can be as big as a forest. A famous example is Pando, a quaking aspen clone in the United States (Mitton and Grant 1996). The individual trees are ramets, and the whole clone is the genet. The genet is often considered to be the fundamental biological individual because it is taken to be the unit of evolution, the entity that confronts natural selection. Pando might also be considered as one physiological individual if we are concerned with the interactions between ramets and how they share nutrients and other molecules and how they send and receive signalling molecules between each other and affect each other’s physiological processes. Tracing the system through rhizomal connections, or in the absence of these, through the mycelial web and even thereby into other plants, it appears that DiFrisco’s criterion provides a boundary that will vary from case to case. Hence it is legitimate, and often appropriate, to consider the genet as one physiological individual for particular research purposes. On the other hand, once again depending on the processes that are under investigation, there may be cases in which it would be better to consider each ramet as one physiological individual.

Suppose we are investigating a volatile signalling molecule in a big genet such as Pando. After the molecule is released, the branches of other trees will receive the signal and plants will respond accordingly. It is likely that this sender-receiver interaction between two ramets which are very close to each other (let’s say ramet A and ramet B) is stronger than the interaction with ramet C on the further end of the genet since distance and the environmental parameters such as wind will reduce the density of the signal. So, in an experiment like this, if ramet C appears to be less clearly a part of the system of which ramets A and B are parts than are A and B, it might be better to say that all the ramets are discrete individuals with varying strengths of pairwise interactions.

It is easy to find usages in which both individual ramets and the complete genet are referred to as individuals. For example, the creosote bush (Larrea tridentata) grows as a ring of clones moving slowly outwards from an initiating plant. It is sometimes claimed that individuals, the entire circular genet, are the longest living organisms on the planet, with continuous growth processes that stretch back over ten thousand years. On the other hand, individual bushes (ramets) are said to live between 100 and 200 years (Vasek 1980). Here we might draw parallels with classically processual phenomena such as rivers. Sometimes we refer to an entire river system as a single entity, sometimes we distinguish (individuate) various tributaries and a central flow. There is no right answer to a question such as “how many rivers are there in the Amazon system?” But note that this doesn’t mean that divisions are arbitrary and unconstrained. We might, for instance have taken the Missouri to be a river continuous with the lower Mississippi, and the upper Mississippi to be a tributary, but we cannot sensibly take the last 100 miles of the lower Mississippi (going upstream) and the first 100 miles of the Missouri as a candidate for a named river. Similarly, we suggest, for ramets and genets.

4 Plant Individuality and Process

Plant physiology provides us with a useful and naturalistic approach for individuating plants, even though it yields multiple physiological individuals that are distinct but also overlapping. The resolution of any apparent tension between the distinctness and plurality of individual boundaries, we propose, is to take seriously the observation that a growing plant is a process, not a thing, and is necessarily, rather than contingently, dynamic. The dynamic interactions between its parts and with its environment are what sustain the plant, maintaining a complex and coordinated structure capable of continued growth.

Waddington (1957) has provided us with an important distinction between homeostatic processes and homeorhetic processes, the former maintaining a specific structure, the latter maintaining a specific trajectory towards a more or less well-defined final state. In the case of animals, we can generally identify homeostasis with short term survival, dependent on metabolism, broadly construed, and behaviour. Homeorhesis, then, is the maintenance of the organism on an approximately determinate developmental pathway. Although we recognise the importance of developmental plasticity, perhaps its decisive importance from an evolutionary perspective, on the individual time scale, it is reasonable to distinguish a developmental norm and the limits of functional developmental variation. The individual, despite important disagreements about its limits, is what persists through the developmental pathway.

One key to understanding plant individuality is to recognise that plants vary considerably in the extent to which they exhibit a normal developmental pathway. While all plants exhibit homeostasis, homeorhesis is much less clear-cut. Here we must distinguish some rather different life history strategies deployed by plants. For many plants, individuality is not significantly more problematic than it is for animals. Almost all plants probably exhibit greater developmental plasticity than almost all animals, but, nonetheless, there is a reasonably clear developmental norm. The clearest cases are perhaps typical annuals, where a single seed goes through a brief life cycle, producing a number of leaves and flowers. The size, shape and form of the whole may vary dramatically in response to soil, light, and other environmental variables, but many factors, especially at the molecular level, will be fairly reliably produced. Many trees, shrubs and perennial herbs may also fit this general picture on longer time scales.

A second case is exemplified by Pando, and applies to many plants for which much or all reproduction is vegetative, or clonal. The homeostatically stable process is clear enough, but homeorhesis is more obscure. For plants like these, it seems that there is no obvious terminus of the life cycle beyond a kind of growth, but a growth that consists in the multiplication of the entities (trees) that we naturally think of as individuals. The natural way of describing the situation in process-ontological terms is as a homeostatic process (genet) with homeorhetic ramets (trees). Living systems with homeostasis but no homeorhesis are best seen as more or less pure process; it is homeorhesis that is the core characteristic of distinct individuals. The ahomeorhetic process may be considered an individual in the way an epidemic or a biological lineage might.¹⁶ It is a process with a particular origin, and all the parts are connected by a similar kind of causal process. The causal process is sustained by the kind of physiological activities we have described. But familiar individuals, with distinctive life histories, are only to be found as the ramets that emerge from this underlying process.

The degree to which such a plant process generates homeorhetically stabilised ramets, finally, is variable. If we think, for example of the ground elder (Aegopodium podagraria), much despised by gardeners, homeorhesis is much less apparent. There are multiple stems emerging from the rhizomal root system, some of which produce flowers. Perhaps the flowering stems look like individuals, but probably no more than individual flowering stems on an individual perennial herb. As we noted at the beginning of this paper, there are plenty of botanical individuals—leaves, flowers, and so on—that are certainly not organism-level individuals, and the flowering stems of Aegopodium surely belong among these. The “organism” is closer to pure distributed process, in which the only individual is the whole process. If we think of the whole lineage as a process, then parts of it are not very interesting individuals, as is readily demonstrated by the fact that they can be created simply by careful deployment of a spade, separating a distinct part of the rhizome mass from the whole. Finally, perhaps further down the route to pure process, we can locate many non-vascular plants such as mosses. These, we suggest, are as much individuals as the individual aspens thrown out by Pando, if a lot shorter lived.

5 Conclusion

The individual plant subjects that are coordinated and sustained by physiological activities are highly diverse. In all cases, there is some diffusion of the individual into the environment constituted by its intimate symbiotic connections with the surrounding microbiota. But the extent to which there are well coordinated individuals beyond the whole growing system is highly variable.

The regulation of source-sink balance in interaction with the environment throughout the life cycle is a distinct aspect of self-organisation in plants. This balance is actively achieved and continuously regulated at every stage of development. Plant parts become sources or sinks or both in different stages of their development, and these transitions are strongly dependent on environmental factors. Given their roles in perceiving the environment, coordinating the body through the life cycle, and responding to the environment, it seems reasonable to say that plant hormones, sugar molecules and other signalling molecules (ion channels, second messengers, receptors) constitute a coordinated system. This system helps us to see plants as individual organisms. These organisms have somewhat vague boundaries and they may be parts of clones, and they may be profoundly intertwined with other symbiotic or conspecific individuals. Plant physiology offers us ways to indicate coordinated plant systems (with vague boundaries) at multiple scales. Depending on the context, their physiological individuality can be as a big as a forest or as small as a little module on a branch.