slime-mould-and-philosophy

Sims
Physarum polycephalum, also known more colloquially as ‘the

blob’, ‘acellular slime mould’, or just ‘slime mould’, is a unicellular
multinucleate protist that has continued to attract the interest
of biologists over the past century because of its complex life
cycle, unique physiology, morphology, and behaviour. More
recently, attention has shifted to Physarum as a model organism The Philosophy
for investigating putative cognitive capacities such as decision of Biology
making, learning, and memory in organisms without nervous
systems. The aim of this Element is to illustrate how Physarum
can be used as a valuable tool for approaching various topics in
the philosophy of biology. Physarum and its behaviour not only
Slime Mould
Slime Mould and Philosophy

pose a challenge to some of the received views of biological
processes but also, I shall argue, provide an opportunity to
clarify and appropriately sharpen the concepts underlying such
received views.
and Philosophy
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Matthew Sims
all of the central topics in the philosophy Michael Ruse
of biology. Contributors to the series Florida State
are cutting-edge researchers who offer University
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from a unique viewpoint.
Cover image: Ascidiae from Kunstformen der Natur (1904)

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Elements in the Philosophy of Biology
edited by
Grant Ramsey
KU Leuven
Michael Ruse
Florida State University
SLIME MOULD AND

PHILOSOPHY
Matthew Sims
Ruhr-Universität Bochum
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DOI: 10.1017/9781009488648
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Elements in the Philosophy of Biology
DOI: 10.1017/9781009488648
First published online: December 2024
Matthew Sims
Ruhr-Universität Bochum
Author for correspondence: Matthew Sims,
matthew.sims-m4e@ruhr-uni-bochum.de
Abstract: Physarum polycephalum, also known more colloquially as

‘the blob’, ‘acellular slime mould’, or just ‘slime mould’, is a unicellular
multinucleate protist that has continued to attract the interest of
biologists over the past century because of its complex life cycle,
unique physiology, morphology, and behaviour. More recently,
attention has shifted to Physarum as a model organism for
investigating putative cognitive capacities such as decision making,
learning, and memory in organisms without nervous systems. The aim
of this Element is to illustrate how Physarum can be used as a valuable
tool for approaching various topics in the philosophy of biology.
Physarum and its behaviour not only pose a challenge to some of the
received views of biological processes but also, I shall argue, provide an
opportunity to clarify and appropriately sharpen the concepts
underlying such received views.
Keywords: slime mould, philosophy of biology, niche construction, biological

individuality, non-neuronal memory
© Matthew Sims 2024

ISBNs: 9781009488624 (HB), 9781009488617 (PB), 9781009488648 (OC)
ISSNs: 2515-1126 (online), 2515-1118 (print)
Contents
1 Introduction 1
2 Niche Construction and Complex Life Cycles 4
3 On the Biotic Status of Spores 25
4 Biological Individuals: A Puzzle Concerning Plasmodial

Fragmenting and Fusing 42
5 Externalised Spatial Memory? 60
6 Conclusion 72
References 75
Slime Mould and Philosophy 1
1 Introduction
Physarum polycephalum (henceforth Physarum), also known more colloquially as
‘the blob’, ‘acellular slime mould’, or simply ‘slime mould’, is a unicellular protist
that has continued to attract the interest of biologists over the past century because
of its complex life cycle, unique physiology, morphology, and behaviour. It has
been used as a model organism for numerous studies, some of which include the
investigation of various mechanisms that underpin synchronous nuclear division,
the development of drugs for the treatment of cancerous tumours, and the investi-
gation of putative cognitive capacities such as decision making, learning, and
memory in organisms that lack nervous systems. More recently, biologists have
even used Physarum to study the effects of microgravity on growth and behaviour
in outer space.
Although Physarum has much to offer in terms of being a model organism
for biological research, as the non-exhaustive list of uses above should make
apparent, the aim of this Element is to illustrate how Physarum can be
a valuable tool for approaching various issues in the philosophy of biology.
Physarum’s unique features not only pose a challenge to some of the received
views of biological processes but also, I shall argue, provide an opportunity to
clarify and appropriately sharpen the concepts underlying such received
views. For example, the notion of ‘niche construction’ has become an important –
yet not fully agreed upon – concept within the context of evolutionary biology.
Roughly, niche construction refers to the idea that evolution is influenced not
only by how (genetic) variation allows organisms to differentially adapt to the
challenges of their environment but also by how organisms modify their
environments and thus alter which selection pressures they are exposed to.
By looking closely at Physarum’s complex life cycle, an opportunity arises to
understand how different kinds of niche construction are exemplified and,
more generally, how those different kinds of niche construction often dynamically
interact.
Each section of this Element is organised around a distinct philosophical issue
as contextualised by Physarum. Using Physarum’s life cycle as a concrete
example, Section 2 focuses on the issue of how attention to complex life cycles
can provide insights into the intricacies of niche construction. Section 3 addresses
the tension between the idea that metabolic exchange is a necessary feature of all
known life and the fact that biologists classify spores as a form of life despite their
being metabolically inert for long periods of time. Section 4 turns to a central
concept in biology – ‘biological individuality’ – and how Physarum’s fragmenta-
tion and fusion behaviour forces us to rethink at least one way of understanding
that concept. Lastly, Section 5 turns to the issue of whether to understand
2 Philosophy of Biology
Physarum’s use of its extracellular slime trails as a form of memory – and if so

whether such memory is subject to explanation in terms of cognition.
In addition to providing a context for investigating various concepts and
puzzling issues in the philosophy of biology, the abundance of empirical research
on Physarum provides a rich resource for constraining how such issues might be
addressed. This is, however, not to say that these issues can be addressed without
philosophically getting one’s hands dirty – they cannot. One additional important
aspect of using Physarum as a tool to approach difficult questions regarding niche
construction, biological individuality, and cognition in non-neuronal organisms is
that many answers can be used to generate testable hypotheses. In other words,
although philosophising is a necessary step in addressing many of these issues, it
is not the only or the last step.
Although I will argue that certain ways of addressing the focal issues brought to
the fore in this Element are more plausible than others, the conceptual revisions
proposed, and conclusions drawn by no means represent anything like a final
word – they are tentative in that they can be both revised and/or overturned on the
basis of further empirical evidence. This kind of openness to empirical amenabil-
ity should not be seen as a defect but should rather be seen as an instance of how
philosophy and biology are a mutually guiding endeavour; an empirically
informed philosophy may be used to generate testable hypotheses and the results
of such hypothesis testing should feed back into altering the very philosophical
accounts which generated the initial hypotheses. This may be seen as an instance
of what Pradeu et al. (2021) have called ‘philosophy in science’ as opposed to
‘philosophy on science’. By throwing into relief some perplexing issues in the
philosophy of biology that P. polycephalum both raises and can be used to
investigate, this Element serves as both an illustration of how this outlier model
organism can be used as a tool for the philosophy of biology, and an invitation for
both philosophers and biologists to do so. Although the aim of this Element is not
to provide a sustained argument for one particular philosophical issue, one might
extrapolate from the useful role that Physarum is shown to play in each section to
the more general claim that advancing the philosophy of biology requires inves-
tigating both typical and atypical model organisms. Concepts and theories based
exclusively on the former may be more intuitive but less representative of the
incredible diversity found in the biological world.
A few preliminary remarks: each section of this Element begins with some
background information that frames the issue at hand and then unpacks the various
details required to grapple with the issue. Given the nature of this Element – a book
centred upon the philosophy of biology – many of the details will involve both
biological descriptions and theoretical concepts: the arsenal of philosophers of
biology. I will do my best, however, to avoid bogging the reader down with any
unnecessary details for fear of not seeing the forest for the trees. There are also
a fair number of figures throughout the Element. These are intended to supplement
some of the more abstract concepts and descriptions that are introduced in each
section. They are by no means intended as replacements for the text.
I have personally been fascinated – unabashedly so – by Physarum and its
behaviour for some years now and I hope this Element can also serve to awaken
a level of fascination for Physarum in both readers who are familiar and those
who are unfamiliar with this organism that is at least on par with my own.
1.1 What Is P. polycephalum?

In order to understand how to use Physarum as a tool, it is important to firstly have
a general understanding of what the proposed tool is. P. polycephalum is an
amoebozoan protist belonging to the class myxomycetes (i.e., the ‘acellular slime
moulds’ or ‘true slime moulds’) (Stephenson and Stempen, 1994) (see Table 1).
It is a eukaryote (i.e., having a nucleus and other membrane-bound organelles),
and like other myxomycetes members, Physarum remains unicellular over the
course of its whole life cycle, developing from an uninucleate cell into
a multinucleate unicellular mass – a ‘plasmodium’.1 In this life cycle stage
transition, Physarum goes from being a microorganism to a bright yellow, giant
cell that is visible with the naked eye (see Figure 1). A species with a broad
geographic distribution, Physarum lives in wooded areas, taking up residence in/
on dead tree stumps and logs that offer the shade, cool temperature, and moisture
it needs to survive. Physarum’s diet consists of living microorganisms such as
Table 1 Taxonomic classification

of P. polycephalum
Domain Eukaryota
Kingdom Protista
Phylum Amoebozoa
Class Myxomycetes
Order Physarales
Family Physaraceae
Genus Physarum
Species P. polycephalum
1
Acellular slime moulds should not be confused with cellular slime moulds of the class
Dictyostelia (e.g., Dictyostelium discoideum). The latter are social amoeba that aggregate at
a stage in their life cycle, forming a multicellular vegetative slug.
Figure 1 P. polycephalum plasmodium: a giant, yellow, unicellular

mass on a log. (Credit: Rich Hoyer. https://creativecommons.org/licenses/
by-sa/3.0/. Unaltered photo). The colour version of this figure is available at
www.cambridge.org/Sims
bacteria, yeast, amoeba, and also decomposing organic matter. Small spore-eating
beetle species, woodlice, land slugs, and other myxomycetes species are among
Physarum’s predators (and more broadly, the predators of myxomycetes).
Physarum – in its plasmodial stage – has proven to be easy to culture in labs
under conditions roughly mimicking those in which it thrives in the wild. This
entails being kept in a humid and dark enclosure and having a steady food supply –
usually store-bought dried oats. In addition to its unique features, the ease with
which Physarum is cultured has added to its popularity as a model organism.
Having a basic understanding of what Physarum is, let us without further ado
put this fascinating organism to work.
2 Niche Construction and Complex Life Cycles

According to Darwinian evolution by natural selection, whether some phenotypes
(i.e., observable traits) are selected for and as a result spread through
a population over time is largely determined by how well those phenotypes
allow individual organisms to cope with environmental selection pressures
they encounter (e.g., predation, changes in food availability, changes in
exposure to physical stressors, etc.). Different kinds of niche construction
may be understood roughly as distinct ways that organisms systematically
affect the selection pressures that they, their offspring, and/or cohabitants
face. Since whether some phenotypes evolve in a population is at least partly

a response to selection pressures as affected by niche construction, under-
standing different kinds of niche construction is required for a more complete
account of evolution by natural selection. This presumably involves not only
understanding how each kind of niche construction is exemplified in isolation
(an abstraction) but also understanding how different kinds of niche construc-
tion interact over time in broader natural contexts.
Using Physarum’s complex life cycle as one such context, the aim of this section
is to investigate different kinds of niche construction and to identify some of the
ways that they are causally related. The broader perspective that niche construction
brings into focus is how organisms not only plastically adapt to their environments
but by doing so also modify their relation to environmental selective pressures in
ways that can potentially affect their own evolution, and/or the evolution of other
taxa which they regularly interact with. By investigating Physarum’s different life
cycle stages and the transitions between them through the lens of niche construc-
tion, the emphasis is placed upon how those stages, given variation in specific
phenotypic parameter values, can go onto influence evolutionary dynamics and are
quite possibly the outcomes of prior niche construction and ongoing evolutionary
dynamics. My aim in this section is not to speculate about any particular role that
a form of niche construction has played in Physarum’s evolutionary history; rather,
it is to exhume the differential importance of different kinds of niche construction
and their causally interweaving relations that are specific to different stages of
Physarum’s complex life cycle. In doing so, this section provides an impetus for
future investigation and modelling of the evolutionary dynamics associated with
the different kinds of niche construction and their relative significance to the stages
of Physarum’s complex life cycle.
I will firstly discuss the concept of niche construction and what it was initially
a response to. I shall then look at the three kinds of niche construction proposed by
Aaby and Ramsey (2019) as a manner of expanding the categories of canonical
niche construction theory. After articulating the notion of complex life cycles,
I will then describe the details of Physarum’s complex multigenerational life
cycle. Lastly, I will turn to the task of identifying both the different kinds of niche
construction as they arise in the various stages of Physarum’s complex life cycle
and how those different kinds of niche construction often dynamically interact
between and within various life cycle stages.
2.1 Niche Construction: An Overview

Beavers use mud, stones, and tree branches to build dams in rivers. This seems
to be common knowledge. However, what are the implications of building dams
for the evolution of those large rodents we know as beavers? By constructing

dams, beavers create small, controlled aquatic pools in which they can easily
access primary food sources and nest. The behaviour of dam-building has been
so effective in contributing to the beaver’s fitness (i.e., survival and fecundity)
that this behavioural phenotype has become characteristic of beavers.2 Moreover,
and importantly, at some point in their evolutionary history beavers developed
other phenotypes that made aquatic life and dam building easier: webbed feet and
a flat, mud-packing tail. In other words, beavers have modified their physical
environments in ways that have affected the impact of selection pressures upon
them, and this in turn has affected which phenotypes have been selected for. Dam
construction on the part of beavers is a paradigm example of niche construction
(or at least one type of it as we shall soon see).
Niche construction is ‘the process whereby organisms, through their metabolism,
their activities, and their choices, modify their own and/or each other’s niches’
(Odling-Smee et al., 2003: 419). From an evolutionary perspective, niches may be
construed as the collection of all selection pressures that populations regularly
encounter (Odling-Smee et al., 2003). Niche construction thus describes how
organisms affect their own (and other’s) evolution. This kind of approach to
evolutionary explanation may be contrasted to those that are known as ‘externalist
explanations’ (Lewontin, 1983) (see also Godfrey-Smith, 1996). Externalist
explanations, it is argued, are founded on the supposition that evolutionary change
is solely an adaptive response to environmental challenges – a supposition that has
found its way in much of neo-Darwinian evolutionary thinking. These explanations
emphasise organismal evolution as a function of the organism and the environment
while simultaneously relegating the environment to a background condition. The
environment, in other words, is viewed as something that is not affected by the
organism in any way that is relevant to evolution.
Departing from explanatory externalism, niche construction stresses the idea
that organisms are active causes of their own evolution.3 Whether it is beavers
modifying their river habitats by constructing dams, burrowing worms altering
the composition of the soil in which they live, or trees shedding leaves and
modifying the soil substrate around them, organisms routinely affect their
selective environment. To this, proponents of niche construction view inherit-
ance as something that outstrips mere genetic inheritance (i.e., the transmission
of DNA across parent–offspring lineages or through bacterial DNA exchange),
2
I will continue to use the term ‘fitness’ to refer to the combination of viability and fecundity,
following the convention of how the term is understood in life history.
3
Some of the key figures in biology and ecology that laid the groundwork for the development of
niche construction theory were Darwin (1881), Clements (1916), Schrödinger (1944), and
Waddington (1969).
acknowledging what is called ‘ecological inheritance’. This refers to ‘the

modified environmental states that niche-constructing organisms bequeath to
their descendants’ (Scott-Phillips et al., 2014: 1233). In acknowledging the
importance of the organism’s impact upon evolution, the niche construction
approach has been viewed as a manner of supplementing standard evolutionary
theory, offering a more complete evolutionary explanation than externalist
explanations can provide alone (Odling-Smee et al., 2003).
Canonical niche construction theory (Laland et al., 2000; Odling-Smee et al.,
2003) recognises two ways that organisms can construct their niches: ‘perturb-
ation’, occurs when organisms modify their physical environment (think of the
beaver and its dam-building); and ‘relocation’, occurs when organisms modify
their spatio-temporal relation to the selective environment (think of birds that
migrate every winter to warmer climates to avoid freezing and/or starvation).
More recently, Bendik Hellem Aaby and Grant Ramsey (2019) have put forth
a tripartite niche construction taxonomy, expanding these two niche construc-
tion categories.4 Although the scope of this section does not permit a detailed
treatment of their arguments, a brief description should serve to make explicit
their rationale for developing the kind of tripartite taxonomy that they put forth.
Firstly, Aaby and Ramsey note that organisms not only relocate to accommo-
date changing resource conditions (e.g., temperature, food, predators, etc.) but
they also often physically change their spatio-temporal relation to other organ-
isms to maintain and control the flow of information between them. For
instance, an antelope might follow a nearby lion in order to remain informed
of its potential predator’s location, thereby reducing its uncertainty about an
attack. This kind of relational modification, although having something in
common with relocation, is not covered by it; it is an indirect epistemic pay-
off that the antelope’s change of spatial location in relation to the lion affords
and not a direct pay-off of escape. Thus, the first line of reasoning motivates
a broadening of the relocation category.
Aaby and Ramsey’s second line of reasoning for an expansion is based upon
the idea that in order for canonical niche construction theory to be consistent
with the notion of niche that it adopts from Odling-Smee et al. (2003), a third
kind of niche construction must be acknowledged. Odling-Smee et al. (2003),
in developing the niche construction approach, deploy Walter J. Bock’s
(1980) factor–feature interactions analysis of niche. According to this analysis,
‘factors’ are selection pressures and ‘features’ are organismal phenotypes. If
a niche consists of the sum of all selection pressures faced by a population, then
4
Also see (Sultan, 2015) and (Chiu, 2019) for similar efforts to expand the categories of canonical
niche construction theory.
this is just to say that a niche consists of the sum of factors faced by a population
that select for organismal features. If something like this is assumed correct,
which it is by canonical niche construction theory, then organisms can alter their
niche in three ways: (1) modifying factors (i.e., perturbation), (2) modifying the
relation between factors and features (e.g., relocation), and (3) modifying their
own features. Thus, for niche construction to be consistent with the factor–feature
interactions conception of niche, constitutive modifications to the features of the
organism must be taken on as a third category of niche construction.
2.2 Three Kinds of Niche Construction

Aaby and Ramsey refer to the various ways (1–3 in the previous paragraph) that
factor–feature relations can be modified, respectively, as external niche construc-
tion, relational niche construction, and constitutive niche construction. External
niche construction (ENC) refers to the modification of the biotic and abiotic
environmental factors made by a focal organism, which thereby changes its
selective environment, that of its offspring, and/or cohabitants. ENC is equivalent
to perturbation of canonical niche construction theory. Paradigmatic examples of
ENC include the construction of dams by beavers or the construction of nests by
birds. Relational niche construction (RNC) refers to the modification of a focal
organism’s spatio-temporal location relative to environmental factors but also the
modification in relation to other organisms which alter a focal organism’s epi-
stemic niche. This latter kind of modification – amongst other things – allows for
the maintenance of information flow from one organism to another and is
particularly crucial for organised social behaviour that is structured according
to a division of labour (Sterelny, 2003). Thus, RNC conceptually includes
relocation but represents a broader category than relocation.
Lastly, constitutive niche construction (CNC) refers to the modification of a
focal organism’s features that alter its causal relation(s) to environmental factors,
and thus alters its (or its offspring and/or cohabitants) relation to selection
pressures.5 CNC occurs via the mechanism of phenotypic plasticity – environ-
mentally induced, non-heritable trait modifications that include reversible and
nonreversible behavioural and morphological changes.6 For instance, a plant,
being sessile, cannot move to a different location if deprived of light. Instead, it
will modify the effects of environmental factors by way of phenotypically plastic
responses, sometimes drastically changing its morphology. This might include
growing broader leaves to compensate for less light or growing narrower leaves to
5
Similar to CNC, the notion of ‘experiential niche construction’ has been extensively developed by
Sultan (2015).
6
Epigenetic modifications are recognised as one of the key molecular mechanisms contributing to
phenotypic plasticity (see Bateson and Gluckman, 2011).
compensate for exposure to excess light (Sultan, 2015). Importantly, such differ-
ences in leaf shape amongst members of the same species are not due to genetic
differences; they are different environmentally induced forms that genetically
identical plants (or the same plant) may take over the course of their (its)
development.
Some proponents of niche construction have expressed scepticism regarding
such an expansion (see Godfrey-Smith, 1996, 2001; Baedke et al., 2021;
Trappes et al., 2022). Part of such scepticism may be seen as stemming from
a general worry concerning the ubiquity of niche construction, namely: if every
selection-relevant biotic or environmental modification that an organism makes
is a form of niche construction, then the concept becomes trivial and of no
explanatory use. Discussing and responding to this criticism, Abby and Ramsey
remind us that both selection and genetic drift are equally ubiquitous phenom-
ena and that this case does not make them any less useful. Their usefulness in
evolutionary theory stems from recognising that not every instance of selection
or drift is equally important in every evolutionary process. That is, there are
explanatory contexts in which specific forms of selection or drift should be
foregrounded, whilst others are backgrounded and this differential importance
across different contexts allows selection and drift to remain useful notions.
According to Abby and Ramsey, niche construction is similar in this manner.
Despite niche construction’s ubiquity, the differential importance of different
types of niche construction relative to a particular explanatory context can help
us to understand and model evolutionary processes. In one particular stage that
makes up Physarum’s complex life cycle (or transitions to and/or from that
stage), a number of different types of niche construction are possibly at play.
However, understanding the differential importance of ENC, RNC, CNC, or
any combination thereof relative to that stage can be useful in understanding
(and informing models of) the evolutionary dynamics that have stabilised that
stage within the sequence of stages that make up Physarum’s life cycle.7
Another worry that some sceptics have raised has to do with the idea that
describing a plastic response in terms of something like CNC fails to provide
any additional information about that response and, thus, to do so is unwar-
ranted. This worry, however, overlooks the fact that although phenotypic
plasticity is a mechanism that underwrites niche construction, considering the
evolutionary consequences of plastic responses is extrinsic to any accurate
description of a response as such. Describing some variable response as
a form of phenotypic plasticity is to acknowledge that it is a change in pheno-
type in response to an environmental or internal cue without any accompanying
7
I would like to thank an anonymous reviewer for pushing me to clarify this point.
genetic change. Although there have been various suggestions that such
responses can have evolutionary impacts on the subsequent genetic fixation of
those phenotypes (West-Eberhard, 2003; Bateson and Gluckman, 2011; Levis
and Pfennig, 2016), that this is the case is above and beyond describing some
response as an instance of phenotypic plasticity. The notion of niche construc-
tion, on the other hand, was formulated in the context of evolutionary theory.
Thus, describing some plastic response as niche construction embeds it in
a broader evolutionary context in which the historical, ongoing, or future
consequences of that response upon evolutionary dynamics is central.
In what follows, I will assume expanding niche construction to include more
than perturbance and relocation is theoretically warranted, enough so to justify
the further exploration of Aaby and Ramsey’s tripartite niche construction
taxonomy. One manner of examining the details of each of the three kinds of
niche construction is to look at how they occur within a life cycle of one
organism. Looking at particular complex life cycles in which all three kinds
of niche construction are present, I shall argue, provides a broad perspective for
examining the details of ENC, RNC, and CNC and the part that each plays in
altering the selective environment of a focal organism. This of course raises the
question of what a complex life cycle is, a topic to which we will now turn.
2.3 Complex Life Cycles

Biologists often explore life cycles to understand the variety of developmental
and reproductive processes that occur from one stage in a generation (such as
a zygote, spore, or larva) to the same stage in the next generation of a particular
species. A ‘life cycle’ is a ‘series of organisational transformations and repro-
ductive phases that lead from a given stage of development of the same
organisational form, to the same stage of development of the same organisa-
tional form in a following generation, through all organisational forms of the
organism’ (Fusco and Minelli, 2019: 23). An organisational form refers to
a distinct type of entity that has its own ontogeny and thus represents a single
generation that undergoes development (Fusco and Minelli, 2019). The life
cycle of, say, a human or an earthworm has a single organisational form that,
through a sequence of developmental processes, is repeated after one gener-
ation. The same is true of metamorphosing beetles and butterflies despite the
fact that the development of a single organisational form consists of various
stages with drastically different phenotypes (the egg, larva, pupa, and adult).
Not all life cycles involve only one organisational form though.
One general feature that biologists use to pick out complex life cycles is
alternation of generations (Fusco and Minelli, 2019). Alternation of generations
refers to a life cycle pattern in which there is an alternation between at least two
different organisational forms with different ploidy levels (haploid or diploid),
each of which also often displays notable differences in morphology, behaviour,
and physiology. Within such a multigenerational life cycle, one generation
produces another with a distinct organisational form, which in turn produces
the next generation of the first type again, marking a return to the beginning of the
life cycle of a different token organism. In this context, production can be
understood as a causal relation (Godfrey-Smith, 2016) in which one entity brings
another entity into existence. This can be contrasted with developing, which is
a continuation or progression from an existing stage, rather than a causal relation.
Alternation of generations is clearly exemplified by plants such as ferns,
mosses, and some algae whose complex life cycles alternate generationally
between two organisational forms: one being a sex cell-producing plant that has
a single set of chromosomes (a haploid gametophyte) and the other a spore-
producing plant with two sets of chromosomes (a diploid sporophyte).8 Each of
these forms represents a distinct generation with its own development and each
organisational form produces the other. In contrast, more recently evolved
animal lineages, including humans and other mammals, exhibit simple, mono-
generational life cycles. Although mammalian reproduction involves haploid
and diploid stages, the haploid stage is limited to gametes (egg or sperm cells)
and does not have its own ontogeny. Thus, neither egg nor sperm qualify as
a separate generation. Through sexual reproduction – more specifically fertil-
isation – adult mammals give rise to a diploid zygote, marking a new gener-
ation. This zygote develops into a diploid adult, resembling its parents. To
stress, haploid mammalian sex cells do not produce the zygote; rather, the
reproducing parents produce the zygote. Nor does the zygote produce the
adult; it develops into an adult.9 In a mammalian life cycle, there is only one
organisational form that develops and gives rise to the same organisational form
of a distinct generation, starting the life cycle anew.
One fascinating example of a complex life cycle, which offers valuable
insights into understanding ENC, RNC, and CNC, and also exemplifies the
potential value of investigating complex life cycles for the purposes of under-
standing niche construction, is that of P. polycephalum. The life cycle of
Physarum involves two vegetative stages, or periods in which there is feeding,
growth, and cellular repair. These stages are the uninucleate ‘ameboflagellate
stage’ and the multinucleate ‘plasmodial stage’. Both stages exhibit distinct
organisational forms and have different ploidy levels (haploid or diploid).
8
For numerous examples, see Fusco and Minelli (2019).
9
The same can be said of complete metamorphosing beetles and sea urchins; a larva in such a case
does not produce an adult but develops into one.
Alternation of generations is apparent in Physarum’s life cycle as ameboflagel-

lates and plasmodia produce each other through characteristic pathways
(Gorman and Wilkins, 1980). This multigenerational haplodiplontic life cycle
features alternating generations of these two vegetative stages.
In addition to these two vegetative stages, Physarum’s life cycle also includes
three dormant stages: ‘the microcyst stage’, ‘the sclerotium stage’, and ‘the
spore stage’. Of these three, only the third is irreversible and represents a non-
optional developmental transition between the plasmodium and ameboflagel-
late. Lastly, there is an obligate and non-reversible ‘fruiting body stage’ which
leads to the spore stage.
I will now briefly describe the journey of P. polycephalum through each of its
life cycle stages, beginning with the spore and ending with the formation of the
spore. I have tried to keep these descriptions brief and to the point; however,
there is a certain level of detail that is required to convey the diverse character-
istics of life cycle stages of an organism like Physarum. These details play
a crucial role in assessing which (if any) of the three different kinds of niche
construction are present in the various stages. I have included Figure 2 as visual
reference. Both the following descriptions and Figure 2 may be revisited while
progressing through the remaining pages of this Element for the purpose of
regaining one’s bearing.
2.4 Stages of Physarum’s Complex Life Cycle

Physarum spores are microscopic dispersal units, consisting of a single haploid
nucleus enclosed within a resistant wall. Separating Physarum’s two vegetative
stages, spores represent a dormant (i.e., metabolically inert) stage that may stay
viable for several years in unfavourable conditions such as drought or cold.
When favourable conditions resume, a spore germinates, producing an amebo-
flagellate cell. The fact that an organisational form distinct from the sporulating
plasmodium (the ameboflagellate) hatches after germination is what makes the
spore an irreversible dormant stage.
The ameboflagellate stage refers to either of two microscopic haploid cell
forms representing the uninucleate vegetative stage of Physarum’s life cycle.
These are the ‘myxamoeba’ and the ‘biflagellate’ forms. As their names
suggest, the former is an amoeboid cell with no fixed shape, while the latter is
an elongated cell with two flagella of different lengths (i.e., hair-like append-
ages that are used for swimming). If spore germination occurs on a surface with
less water content, the result will be a myxamoeba cell. However, when spore
germination occurs in free water, this results in the hatching of a biflagellate cell
(Clark and Haskins, 2016).
Figure 2 Stages of P. polycephalum’s complex life cycle: (1) spore;

(2) germinating spore; (3) ameboflagellate: myxamoeba above and biflagellate
below; (4) microcyst; (5) ameboflagellate fusion: myxamoeba fusion on the
right and biflagellate fusion on the left; (6) fused cells prior to nuclear fusion;
(7) nuclear fusion; (8) early plasmodial cell after nuclear mitosis without
cell division; (9) mature plasmodium; (10) sclerotium; (11) commitment to
fruiting stage; (12) fruiting bodies. Haploid and diploid stages indicated by grey
arrows and black arrows, respectively. Illustration by Guido I. Prieto
(2024) adapted from Stephenson and Stempen (1994).
Myxamoebae locomote on surfaces by pulling and pushing themselves with

temporary, arm-like projections called ‘pseudopods’. They feed upon fungal
spores, bacteria, and other microorganisms via phagocytosis and reproduce through
binary fission (Clark and Haskins, 2015). During division, however, myxamoebae
cannot feed (Collins, 1979). Successive divisions result in a colony of genetic
clones. If a myxamoeba becomes submerged in free water, it rapidly transforms
into a swimming, biflagellate cell. Biflagellates may feed but cannot undergo binary
fission (Clark and Haskins, 2015). Upon encountering drier conditions, the bifla-
gellate will rapidly revert into a myxamoeba again. This highly plastic cell trans-
formation can occur multiple times in either direction, depending upon the
availability of free water (Pagh and Adelman, 1988).
Under unfavourable conditions such as starvation, drought, overabundance
of water, and overcrowding, the ameboflagellate may convert into a dormant
microcyst. This resistant structure, a suspension of vegetative growth, can
remain viable for long periods of time. Encysting of the ameboflagellate
involves the synthesis of a resistant wall around the cell, in addition to various
other intracellular changes (Gorman and Wilkins, 1980). In contrast to the
spore, the microcyst is a reversable dormant stage; when environmental
conditions improve, it reverts into ameboflagellate again.
Upon encountering another mating competent cell of a compatible mating
type, two haploid myxamoebae (or two biflagellate cells) may sexually fuse.
This leads to the initiation of the plasmodium stage, in which nuclear fusion
and the subsequent formation of a diploid zygote cell occur. As the diploid
nucleus undergoes multiple rounds of division without cell division, the cell
grows and develops into a multinucleate plasmodium, the other vegetative stage
of Physarum’s life cycle. It is during this stage that Physarum becomes visible to
the naked eye as a mass of bright yellow, slimy protoplasm. It may reach a size
of up to 900 cm2 and can crawl across surfaces at a speed of up to 5 cm/h
(Kessler, 1982).
As it grows, the plasmodium migrates across decaying organic substrates,
feeding and avoiding any environmental conditions that may challenge its
viability. Plasmodia consume bacteria, fungi, and other microbes (including
other myxomycete amoebae), but can also feed on non-living organic matter.
Feeding occurs in this stage via both phagocytosis and the excretion of enzymes
that break down organic matter which is then absorbed into the cell (Bailey,
1997). The cell’s shape is plastically reorganised on the go via the restructuring
of an internal, vein-like tubular network, through which protoplasm is rhyth-
mically shuttled. Such shuttling pushes the edges of the cell towards food or
away from potentially harmful substances. As it migrates, a trail of extracellular
slime (i.e., a non-living, cytoplasmic casing) is secreted which, amongst other
things, functions as a lubricating surface upon which to crawl more easily
(Patino-Ramirez et al., 2019). Upon encountering a patch where nutrient condi-
tions are adequate, plasmodium may remain sedentary, growing steadily at that
location (Dussutour et al., 2010).
When encountering adverse conditions such as prolonged periods of drought,
starvation, and/or low temperatures, a plasmodium may transform into a dried,
hard, resistant mass called the ‘sclerotium’ (plural: sclerotia). Like the micro-
cyst, the sclerotium represents a reversible dormant structure, the formation of
which allows a plasmodium to withstand unfavourable growth and metabolic
conditions until those conditions subside. A plasmodium can remain dormant as
sclerotium anywhere from months to years (Sperry et al., 2022). When condi-
tions improve, the sclerotium may revert back into a plasmodium and continue
living as a large diploid vegetative cell. Like the microcyst, the sclerotium is
also an optional developmental stage; whether it occurs in an individual
Physarum’s life cycle will depend upon the kinds of environmental conditions
which are encountered by the individual plasmodium.
Within a period of extended starvation, a mature plasmodium will migrate from
its usual shaded microhabitat into the light, where various biochemical events
lead to the differentiation of the cell protoplasm into multiple fruiting bodies or
‘sporangia’ (singular: sporangium) (Gorman and Wilkins, 1980). Physarum’s
sporangia consist of long, thin, twisted stalks upon which multiheaded spore
enclosures are attached: hence the species name ‘polycephalum’ (many-headed).
Once the process of fruiting has begun, it is irreversible. During spore develop-
ment, meiotic cell division occurs, resulting in the formation of multiple uni-
nucleate spores within the spore enclosure. After a period in which fruiting bodies
and their spore contents dry, spores are released and dispersed by wind or also
sometimes via surface contact with spore-eating arthropods (Blackwell, 1984;
Sugiura et al., 2019). This completes Physarum’s complex life cycle.
How might the various stages of Physarum’s life cycle provide concrete
examples of either ENC, RNC, or CNC, and how might these forms of niche
construction work in tandem? This is the topic to which we will now turn.
2.5 Three Kinds of Niche Construction Exemplified

in Physarum’s Life Cycle
Recall, Aaby and Ramsey’s tripartite niche construction taxonomy: ENC is the
modification of an organism’s environmental factors; RNC is the modification
of an organism’s spatio-temporal relation to environmental factors and other
organisms; CNC is the modification of an organism’s features that alter its
causal relation(s) to environmental factors. Importantly, ENC, RNC, and CNC
are forms of niche construction because an organism’s engaging in any of them
may influence the impact of selection pressures and hence affect fitness and
evolution. Now let’s consider how these various kinds of niche construction
may figure into some of the stages of Physarum’s life cycle. I will focus upon
Physarum’s two vegetative stages – optional dormant stages, and the fruiting
body stage – because I find them to be the most revealing in terms of how
ENC, RNC, and CNC interact across development. The examples of niche
construction that I identify here are not meant in any way to be exhaustive;
within the various stages of Physarum’s life cycle there are undoubtedly many
more instances of niche construction that occur. For reasons of space, I cannot
deal with all of them here.
Starting with the reversible and optional transformation from myxamoeba to
biflagellate, I would like to argue that this transformation provides an example of
both CNC and RNC. To see this, consider that a myxamoeba is limited to the use
of pseudopods for locomotion and hence cannot swim (or at least cannot swim
effectively). As such, the presence of free water introduces a fitness-relevant
challenge: assuming that capturing food in water requires effective locomotion,
a submerged myxamoeba may be less successful at capturing food than it would
be in a non-water microhabitat. The ability to transform into a biflagellate medi-
ates this challenge. Although the degree that a biflagellate cell can direct its
movement is very limited and the distance that it can swim is typically short,
being able to swim can improve feeding in some situations (Clark and Haskins,
2015). In morphologically transforming from a myxamoeba to a swimming
biflagellate, the ameboflagellate increases the amount of food available to it
while it is in its water microhabitat. Moreover, because biflagellate cells cannot
undergo binary fission, and feeding cannot occur at the same time as binary
fission, a biflagellate may continue to feed without interruption as long as food is
available. In short, the water-induced transformation from myxamoeba to bifla-
gellate is an active modification of the ameboflagellate’s features that change its
causal relation(s) to environmental factors. This is a clear instance of CNC, one
that albeit occurs in a motile organism.
The transformation into a biflagellate, however, comes with a potential
fitness cost since of the two ameboflagellate forms only the myxamoeba can
undergo binary fission and produce daughter cells. As such, a sustained exist-
ence as a biflagellate means low ameboflagellate fecundity. Transforming into
a biflagellate thus seems to mediate one kind of selection pressure but in turn
introduces another: the inability to reproduce as a biflagellate cell. One manner
of accommodating this morphology-related decline in fitness is for the amebo-
flagellate to swim to a dry surface (if the surface is not too far away), thus
changing its spatial relation to the water microhabitat that induced its current
form. This active change in location on the part of the ameboflagellate repre-
sents an instance of RNC, which in addition to the subsequent reversion to the
myxamoeba form – an instance of CNC – re-establishes the ameboflagellate’s
ability to undergo binary fission again.
The transformation from myxamoeba to biflagellate and back exemplifies not
only CNC and RNC but also an interesting way that these two kinds of niche
construction are related: CNC may allow an organism to temporarily compen-

sate for the effects of changing environmental factors via plastic phenotypic
modification (e.g., transforming into a biflagellate swimming cell and as a result
being able to capture more food) and in some cases, the same CNC-based
phenotypic modification may also allow an organism to change its relation to
the CNC-inducing environmental factor(s) (e.g., flagella propelled swimming
allowing a cell to relocate to a dry surface). This locational change is
a straightforward case of RNC, the coming about of which is not only causally
enabled by the phenotypic change brought on by an initial instance of CNC but
is also a response to the cost of that phenotypic change (e.g., having zero
fecundity as a biflagellate). Actively engaging in RNC may, in turn, result in
a subsequent instance of CNC occurring (e.g., reversion to a myxamoeba), both
jointly restoring the organism’s causal relation to environmental factors in
a way that has potential fitness effects.
The microcyst stage, I would like to suggest, represents an instance of CNC.
Recall that the microcyst is a reversible and optional dormant stage that may
interrupt the ameboflagellate stage, provided that the cell encounters
unfavourable environmental conditions. For example, when a myxamoeba
fails to encounter nutrient resources for an extended period of time or when its
immediate environment becomes too dry for long periods of time, these
conditions induce the encysting of the cell. Encysting consists of the forma-
tion of a resistant cell wall around the ameboflagellate that protects it from
potentially harmful environmental factors, allowing it to enter a non-
vegetative stage in which energy is radically conserved (Stephenson and
Stempen, 1994). Microcyst formation allows the ameboflagellate to maintain
its viability in a dormant state until favourable environmental factors are
detected and the cell can resume its vegetative existence. Like the transform-
ation from myxamoeba to biflagellate, becoming a microcyst trades fecundity
for viability as long as dormancy is maintained. Importantly, exiting the
dormant microcyst stage is highly responsive to changes in environmental
conditions (Clark and Haskins, 2015). The mechanisms underwriting the
conjunction of encysting and excysting can be viewed as determining the
selective environment that will be experienced by the ameboflagellate: if
conditions are good, revive so as to affect and be affected by those conditions;
if conditions remain bad, remain dormant and beyond the reach of those bad
conditions. The reversible transformation into a microcyst may thus be viewed
as a radical yet temporary modification of organismal features that change the
cell’s relation to environmental factors. Given Aaby and Ramsey’s character-
isation of CNC, entering and exiting the microcyst stage exemplifies an
instance of CNC.
The microcysts stage is also an optional manner that an ameboflagellate can

change its spatio-temporal relation to other colony members and, hence,
a revealing case of RNC. One way for an organism to change its spatio-
temporal relation with other organisms is to move towards or away from
those organisms; another way is for an organism to remain fixed while other
organisms spread out. This latter kind of relational change is particularly
relevant for myxamoebae, which find themselves in an overcrowded colony.
If all myxamoeba cells in a colony do not encyst (but a fair number do) due to
overcrowding, then a locationally fixed encysting cell may experience reduced
resource competition at a later time (i.e., exiting dormancy to fewer cohabitant
cells). Moreover, by interrupting their ameboflagellate vegetative stage, encyst-
ing cells immediately reduce competition for those cells in the colony that do
not encyst. Thus, I would like to suggest that entering and exiting the microcyst
stage can be construed as an instance of RNC mediated by CNC.10
The plasmodium’s production and use of extracellular slime that is charac-
teristic of this stage represents a paradigmatic example of ENC. To see how,
recall that a motile, foraging plasmodium leaves behind an extracellular slime
(mucopolysaccharide) trail wherever it migrates. Slime trails are often (but not
always) avoided by plasmodia (Reid et al., 2013). Not unlike Hansel and
Gretel’s breadcrumbs trails, the scattering and following of which allowed
them to find their way out of the forest, extracellular slime trails may sometimes
be used by a plasmodium as a cue for avoiding previously foraged locations
(Smith-Ferguson et al., 2017). This allows a plasmodium to both avoid spending
its metabolic resources on (re)visiting areas that are not likely to contain food
and, as a result, reach patches containing food faster than it would without the
aid of extracellular slime (Reid et al., 2012) (see Section 5). This two-way
causal interaction between a plasmodium and its extracellular slime (or the
slime trails of other plasmodia) exemplifies how changes made to the physical
environment (i.e., extracellular slime trails) can act as feedback so as to
constrain a plasmodium’s foraging behaviour and thereby change the selection
pressures impacting it and/or its conspecifics. A plasmodium’s interaction with
its extracellular slime reduces the amount of time and energy spent on foraging
in complex environments, something which may have direct fitness effects.
Given that the inability to detect and follow slime trails has negative fitness
effects, we might expect (a) any individuals in the population that fail to be able
10
If the timing of encysting and excysting is influenced by genetic variation, and either encysting
or excysting too early or too late can have negative fitness effects, then selection for those
variations on timing mechanisms that are tuned to the onset and termination of unfavourable
environmental conditions may occur. As such, variation in timing mechanisms underwriting
when CNC-mediated RNC occurs can have effects on subsequent evolution.
to exercise this capacity would be outcompeted and (b) that any heritable
genetic variations that would allow Physarum to exercise this capacity would
be maintained in the population.
The production and use of extracellular slime may also provide a possible
example of how ENC and RNC occur in tandem. Whether a plasmodium avoids
slime trails will be dependent upon things like the presence and quality of food
that can be reached by migrating across extracellular slime (Reid et al., 2013)
and/or the nature of biochemical cues reflecting the stressed or well-nourished
condition of the plasmodium that left the slime trail (Briard et al., 2020). If
a well-nourished plasmodium leaves behind a carbohydrate-rich slime trail and
such trails provide nutrients for the growth of red yeast, then a well-nourished
plasmodium may also eventually revisit its own slime trail to consume the red
yeast that have since grown there (Epstein et al., 2021). This plasmodial fungal
farming – if it is indeed a robust phenomenon – seems to be both an instance of
ENC and RNC;11 it is both an active modification of environmental factors (i.e.,
leaving slime trails) that impact selection pressures (i.e., the availability of food)
because it influences the spatio-temporal relation between the slime-secreting
plasmodium and the growing red yeast. In other words, ENC has the fitness
effects that it does because it brings about RNC. The fact that a plasmodium will
choose to consume higher quality food over lower quality food (Latty and
Beekman, 2010) when there is an option may thus allow it to modify its physical
environment with extracellular slime trails in a way that, over time, systematic-
ally alters its relationship to the fungi which it consumes; a well-nourished
plasmodium brings yeast to it (locally), rather than having to relocate to yeast
elsewhere.
When a plasmodium migrates from a food-depleted to a food-abundant site in
the same habitat, such migration depends upon its ability to plastically modify its
features. During the plasmodial stage, a Physarum is able to change its shape by
altering its internal tubular network structure in a matter of hours in response to
changes in external conditions (Nakagaki et al., 2004). This structural reconfig-
uration that alters the way plasmodia experience their heterogeneous resource
environment as more homogeneous is analogous to how plants modify their root
structure according to changing soil nutrient patch availability (one exception
being that plants are sessile and operating at a much slower timescale than
plasmodia). And like such plant root reconfiguration may be viewed as an
11
I make this qualification because the oscillatory successional dynamics that Epstein et al. (2021)
discovered were based upon an analysis of only five Petri dish ‘ecosystems’, each of which
differed in experimental light exposure conditions. To show that plasmodial yeast farming is
a robust phenomenon, this experiment requires replication using many more samples of each
ecosystem condition.
instance of CNC, so may the structural modification of a plasmodium in response

to fluctuation in food availability.
The fact that plasmodial structural reconfiguration in response to resource
fluctuation may be viewed as an instance of CNC has an interesting upshot for
understanding the phenomenon of yeast farming: such farming may be viewed as
a dynamic process involving organismal feature modification (i.e., tubular net-
work restructuring), environmental factor modification (i.e., secreting slime
trails), and modification of spatio-temporal relations between the focal organism
and another organism (i.e., changing the relation between slime-secreting plas-
modium and growing red yeast). Hence, a more complete (but most likely non-
exhaustive) analysis of Physarum yeast farming from the perspective of niche
construction might be the following: CNC brings about ENC, which results in
RNC, and RNC in turn brings about CNC, resulting in ENC, and so on. This
continuous cycle of factor–feature codetermination is maintained as long as the
successional dynamics between a plasmodium and yeast colonies are.
What of the sclerotium stage? Might it too exemplify a form of niche
construction? Recall that the sclerotium is an optional and reversible dormant
stage which is elicited by encountering unfavourable vegetative conditions.
Entering this stage involves a dramatic plasmodial cellular modification that
includes the encrustation of the protoplasm in addition to various cytological
changes allowing for stored energy reserves to be used (Gorman and Wilkins,
1980). Both entering and exiting the sclerotium stage, similar to entering and
exiting the microcyst stage, may be viewed as instances of CNC. In transform-
ing into a sclerotium and thus enabling a plasmodium to use stored metabolic
resources, a resource-poor environment for a plasmodium becomes a resource-
indifferent environment for a sclerotised cell; starvation or drought becomes
less relevant to viability maintenance whilst in this stage. Here again, we find
a temporary fitness trade-off between fecundity and viability; as long as the
plasmodium remains dormant as a sclerotium, it cannot reproduce (i.e., sporu-
late) but it can remain viable for up to years in conditions that would be
deleterious for the non-resistant vegetative plasmodial cell. The sclerotium, in
reverting back to a plasmodium under favourable environmental conditions,
both regains the ability to commit to sporulation and also becomes once again
constrained by the metabolic needs of a vegetative cell.
Lastly, by migrating into the light, a mature and starving plasmodium initiates
the process of differentiation, whereby its protoplasm (and protoplasmic con-
tents) becomes distinct fruiting body parts (i.e., the base, the stalk, the spore
case, the spores). This process, in turn, culminates in cessation of the vegetative
plasmodium and genesis of the multiple reproductive units: haploid spores. Can
this transformation from a plasmodium into fruiting bodies be plausibly viewed
as a kind of niche construction? Although not as straightforward as the previous

examples, this transformation may represent an interesting case of ENC via
organismal feature modification, albeit a feature modification that does not
qualify as CNC. That the fruiting body stage is irreversible suggests that it is
not a means for an individual plasmodium to buffer itself against unfavourable
environmental conditions; rather, it is a necessary step along the way to repro-
duction. This transformation does not change the causal relation of the plasmo-
dium qua fruiting body to selection pressures because transforming into
a fruiting body coincides with the termination of the plasmodium. Thus,
although the transformation into a fruiting body is a radical modification of
the plasmodium’s features, it fails to be an instance of CNC.
Fruiting bodies are differentiated physical structures made by and from the
plasmodium in support of the development and dispersal of spores (Keller et al.,
2008). As such, spore number may be viewed as a (potential) measure of
a plasmodium’s fecundity, and maturing fruiting bodies are a change made to
the physical environment by the pre-fruiting plasmodium in realising its
fecundity. Fruiting body formation thus may be viewed as a kind of ENC, one
that affects how the next generation of ameboflagellates experience their envir-
onment by affecting mature spore dispersal. For instance, in comparison to
fruiting bodies with shorter stalks, those plasmodia that produce fruiting bodies
with taller stalks may be more effective at both protecting the encased spores
from excessive moisture and contributing to the dissemination of the dry spore
mass because spores are elevated higher above the substratum (Keller et al.,
2008). Insofar as such fruiting body character variation (i.e., having taller or
shorter stalks) is determined by the genome (and possibly heritable epigenome)
of the pre-fruiting plasmodium, such variation is subject to natural selection.
A plasmodium’s fruiting so as to lift its spores higher off the substrate and
indirectly affect spore dispersal is a form of (canalised) ENC-mediated RNC.
External niche construction in one generation of entity (the plasmodium), rather
than having effects upon the selection pressures which it faces, impacts which
selective environment is faced by a subsequent generation of entities with
a distinct organisational form (ameboflagellates).
The fruiting body stage, hence, illustrates how ENC-mediated RNC may
have effects upon the next generation without such effects being mediated by
ecological inheritance. Like a bird’s nest, the fruiting body surrounding the
spores is a fleeting structure. It is neither used, maintained, nor cumulatively
built upon by ameboflagellates or the following generation of plasmodial cells.
The characteristics of the mature fruiting body which make it the environmental
factor that it is nonetheless affect which subsequent factors of the selective
environment that ameboflagellates experience.
Taking stock: I have illustrated how some of the stages that P. polycephalum
completes over the course of its complex life cycle exemplify at least one of the
three kinds of niche construction included in Aaby and Ramsey’s (2022)
tripartite niche construction taxonomy. Moreover, I have shown how some of
these stages and the transitions between them reveal different ways that ENC,
RNC, and CNC causally interact and occur in tandem. Lastly, I have shown how
some of the (reversible and non-reversible) transitions between Physarum’s life
cycle stages associated with CNC and ENC can be viewed in terms of fitness
trade-offs (see Table 2). I will now offer a few considerations regarding the
value of looking at complex life cycles for niche construction approaches.
2.6 The Value of Looking at Complex Life Cycles

for Niche Construction
What does examining various kinds of niche construction in the context of
complex life cycles tell us that looking at them outside such a context cannot?
One immediate answer to this question is that complex life cycles provide
a broader context in which to explore how different kinds of niche construction
interact in a dynamic manner. For example, relation between kinds of niche
construction, patterns amongst those relations, and where those patterns arise in
one organism’s complex life cycle can be used to probe for the presence of such
relations and patterns in other taxa. Doing so, would allow niche construction
practitioners to confirm either the generalisable nature of such patterns or
investigate how such patterns differ due to differences in ecological and life
history characteristics (e.g., differences in habitat/microhabitat, trophic rela-
tions, reproductive modes and schedules, number of generations within a life
cycle, growth rate, dormancy patterns, etc.). Importantly, some of these gener-
alisable patterns may be particular to complex life cycles.
Assuming that looking at niche construction by way of simple life cycles can
often reveal complex relations that investigating an individual instance of niche
construction in isolation cannot, complex life cycles may potentially offer an
even richer source of niche construction-relevant phenomena and relations
amongst them to investigate. This is due to their being multigenerational and
featuring more than one reproductive and/or nuclear phase. For example,
although CNC-mediated RNC or RNC-mediated CNC may be relations that
are also found in some simple life cycles, the question as to how CNC-mediated
RNC and RNC-mediated CNC are sequentially organised within the same life
cycle is something that is much more amenable to investigation using complex
life cycles. This is because life cycles featuring alternation of generations are
more likely to be those that feature both kinds of relation and thus identifying
Table 2 Life cycle stages of P. polycephalum (excluding the spore stage), some of the kinds of niche construction
arising within and/or between them, and the resulting fitness trade-offs. If there are relations between kinds of niche construction
exhibited in the sclerotium stage and/or whether there are fitness trade-offs in the plasmodium stage have not been
addressed in the analysis above and remain open questions for future research
Life cycle Relations between niche

stages Types of niche construction construction types Fitness trade-offs
Ameboflagellate Constitutive: interconvertible transformation Relational mediated constitutive niche Temporarily
from and to myxamoeba and biflagellate construction: relational niche construction suspending
in response to the presence or absence of as a means of bringing about subsequent fecundity to
free water constitutive niche construction. maintain viability
Relational: a biflagellate’s swimming to (as biflagellate)
a dry substrate from a water microhabitat,
resuming the ability to asexually
reproduce as a myxamoeba
Microcyst Constitutive: optional and reversible Constitutive mediated relational niche Temporarily
transformation from ameboflagellate to construction: constitutive niche suspending
resistant, dormant unit in response to construction as a means of bringing about fecundity to
drought, abundance of metabolic by- subsequent relational niche construction. maintain viability
products, overabundance of cells, and/or
starvation
Relational: encysting that alters the
spatio-temporal relation of the
ameboflagellate to other cells in the
colony, possibly reducing resource
competition
Table 2 (cont.)
Life cycle Relations between niche

stages Types of niche construction construction types Fitness trade-offs
Plasmodium External: depositing and using extracellular Cyclical niche construction: constitutive ?
slime for improved navigation and niche construction brings about external
efficient foraging in complex niche construction, which results in
environments relational niche construction that in turn
Relational: allowing red yeast to grow on brings about further constitutive niche
deposited carbohydrate-rich extracellular construction and more of the same
slime for later consumption
Constitutive: structural reconfiguration of
the internal network of tubes in response to
resource fluctuation
Sclerotium Constitutive: optional and reversible ? Temporarily
transformation from plasmodium to suspending
resistant, dormant unit in response to fecundity to
drought, light, and/or starvation maintain viability
Fruiting Body External: plasmodial transformation into External mediated relational niche Permanently
partially non-living environmental construction: external niche construction suspending viability
structures that support the development as a means of bringing about relational for fitness of next
and dispersal of spores niche construction in next generation generation
patterns between those relations becomes possible in such a context. To stress,

I am not suggesting that investigating niche construction should proceed by
exclusively investigating complex life cycles. To the contrary, I am suggesting
a pluralist approach that urges a supplementary use of complex life cycles to
buttress and fill out investigations of niche construction that have focused
exclusively upon individual instances of feature–factor modification outside
of the broader context of (simple or complex) life cycles.
In this section, I have used Physarum’s life cycle to exemplify how complex
multigenerational life cycles, despite being biological phenomena that may at
first glance seem unrelated to niche construction, can be used as a valuable
manner of investigating niche construction. In Section 3, we shall take a closer
look at Physarum’s spores, considering a puzzle that is to do with the fact that
dormant spores lack one of the features that many biologists agree is character-
istic of life on Earth – metabolism – and are yet considered an example of life.
3 On the Biotic Status of Spores

There have been numerous theories of life proposed by different biologists and
philosophers, many of which have been partially (if not wholly) motivated
by a desire to understand the origins of life on Earth, the possible forms of life
beyond Earth, and/or the relationship between life and cognition (Cleland, 2019).
When one asks, ‘what is life?’, one common way of going about investigating this
question is to ask, ‘what makes some entity a living system?’ – that entity being any
acknowledged example of life. Answering the latter question is supposed to
shed light on the former – the former presupposing some agreement about
examples of life and asking what properties those examples have in common.
Let’s call the general view that questions about life are questions about living
(and vice versa) ‘life-living equivalence’. Some prominent theories, assuming
life-living equivalence, have looked to reproduction and active metabolic
exchange processes as necessary but non-sufficient conditions for being
a living system and, hence, being necessary for life as we know it. While
non-reproducing, yet unarguably living, mules present at least one counter-
example to the notion that reproduction is necessary for life, in this section, I will
focus exclusively upon metabolic exchange and how attention to the biotic status
of dormant spores (i.e., whether they qualify as living, dead, or as some other
living-related state) might bring some clarity to the concept of life.
Since dormant spores neither take in energy resources from their environ-
ment nor output waste, they are metabolically inert entities. Despite being
metabolically inert, spores are recognised by biologists as an example of life.
Such explicit recognition is clear, for instance, on NASA’s Office of Safety &
Mission Assurance (OSMS) webpage, where they write on bacterial spores:
‘Spores are the most likely form of terrestrial life to be able to survive on
another planet’ https://sma.nasa.gov/sma-disciplines/planetary-protection/
explore/explore-item/what-are-spores.
That biologists also view spores as exemplifying life is evidenced by the fact
that they are regarded as stages in life cycles of spore-forming organisms
(Section 2.2). It would be truly odd if spores were considered devoid of life
and yet featured as a developmental stage within a life cycle.
The claims that dormant spores are an example of life and that a living system
must necessarily engage in metabolic processes, however, pull in different
directions when assuming life-living equivalence. For if spores are an example
of life, then, deploying life-living equivalence, they are also living systems.
However, in taking the assumption onboard that metabolic activity is necessary
for life, spores also turn out to be non-living systems because they do not engage
in metabolic activity. Taken together, we arrive at the conclusion that dormant
spores are both living systems and non-living systems. Two ways of avoiding
this reductio ad absurdum that make sense of the fact that biologists regard
dormant spores as an example of life are to: (1) maintain life-living equivalence
and relax the condition that metabolic exchange is necessary for being a living
system or (2) keep the condition that metabolic exchange is necessary for being
a living system and abandon life-living equivalence.
In this section, I will build a case for the second option, arguing that the relevant
equivalence is between life and being alive (rather than life and living), and that
living is a way of being alive. To illustrate and develop this position I will articulate
a taxonomical analysis of the biotic status of Physarum spores – an analysis that can
be generalised to other spore-forming taxa given the shared biotic features of
spores. This section will have the following organisation: firstly, I will survey
some examples of metabolic definitions of life that have been introduced in biology
(and biology-related fields), highlighting how these definitions deploy life-living
equivalence and, hence, assume that engaging in metabolic exchange is not only
necessary for being a living system but also necessary for life. Turning to Physarum
spores, I will briefly look at their metabolic inert (dormant) state and then articulate
one reason why biologists consider ametabolic dormant spores an example of life.
Nick Lane’s (2016) distinction between ‘living’ and ‘being alive’ will then be
elucidated and used as the basis for taxonomising the biotic status of Physarum’s
spores (and spores of other taxa) in support of option (2). Lastly, I will deploy the
proposed taxonomy to consider spore ageing and its relation to senescence in
vegetative entities, illustrating one of the wider implications of this taxonomy.
3.1 Is Metabolism a Requirement for Life?

Amongst the various ways that life has been conceptualised, the idea that metabol-
ism is a necessary component of life has been central to many of them. Spelling this
out has usually, but not always, taken the form of defining life in terms of
metabolism, where such definitions are based upon the examples of life that we
have observed on Earth. Setting aside the obvious problem of basing a definition of
universal life (i.e., life on Earth and beyond) upon a sample of one (i.e., earthly life)
(Cleland, 2018), in what follows I shall only be interested in what can be said about
life as we know it – on Earth. Whether there is reason to believe that life on Earth is
representative of life everywhere will not be taken up here. Some of the metabolic
definitions and characterisations of life that have been previously suggested will be
used as a jumping-off point to illustrate that many biologists view metabolism as
a necessary condition for life and that questions about life are often equated with
questions about living (i.e., life-living equivalence).
So, what is metabolism? Metabolism may be characterised as the sum of all
biochemical processes by which a system extracts energy from its environ-
ment, uses that energy in a controlled fashion to maintain its organisation
despite the material turnover of its component parts, and produces metabolic
waste. Metabolism is typically understood as consisting of two processes:
‘catabolism’ and ‘anabolism’. Catabolism is the breaking down of energy
resources (e.g., carbohydrates from food), releasing energy contained in
chemical bonds. Anabolism is the use of that released energy for cellular
function, growth, and repair via the synthesis of proteins, nucleic acids, and
adenosine triphosphate (ATP).12 As such, catabolism and anabolism can be
viewed as converse and yet coupled reactions, the former producing energy
for use and the latter using energy for further energy production. Metabolism
also involves making waste products. Metabolic waste is any surplus and/or
toxic by-product of metabolic reactions that cannot be used for the mainten-
ance of cellular function. These products take the form of solid, liquid,
gaseous, and heat products, and are returned to the environment in ways that
are often powered by metabolism. I will use ‘metabolic exchange’ as shorthand to
refer to the combination of all of these processes.
How might metabolic exchange feature into a definition of life? Carl Sagan,
providing an overview (and also a stinging critique) of various definitions of life
in his now-classic Encyclopaedia Britannica entry ‘Definitions of Life’,
describes a standard metabolic definition of life as one based upon the idea that
12
ATP is an energy-supplying molecule that is often referred to as the cellular ‘energy currency’
because its breakdown via catabolism supplies a source of energy that is used for the vast
majority of cellular functions.
a living system is an object with a definite boundary, continually exchanging

some of its materials with its surroundings, but without altering its general
properties at least over some period of time. (Sagan, [1970] 2010: 303)
A living system, according to this definition, is one that is delimited by

a boundary (e.g., a membrane, cell wall, etc.) and that continuously engages
in metabolic exchange with its environment. Although a boundary is not an
explicit feature of metabolic exchange, it is something that many metabolic
definitions of life feature. One reason for this is that boundaries provide a way of
controlling what happens on the inside of that boundary – not everything gets in
or out. Similarly, the idea that a system exchanges energy and waste with its
environment is premised upon it – the system – having a boundary that separates
it from its environment. Sagan’s definition also highlights the idea that a living
system’s general properties remain unaltered (at least for a while) despite the
ongoing metabolic exchange that occurs.
Autopoetic theory offers another example of how metabolism is considered to
be a defining feature of living systems. Autopoetic definitions are admittedly
abstract, tending to focus upon the organisational logic of circular ‘self-
production’ (Maturana and Varela, 1980). This is the idea that metabolic pro-
cesses, and hence living processes, are those that circularly produce the system’s
organisation and are produced by the system’s organisation. This kind of recur-
sive self-production, according to autopoietic theory, is responsible for the self-
sustaining property that is particular to living systems; it explains their autonomy,
something that distinguishes them from inanimate or dead systems. Interpreting
Maturana and Varela (1973), philosopher Michael Bitbol and biochemist Pier
Luigi Luisi provide the following autopoietic definition of life:
[L]ife is a cyclic process that produces the components that in turn self-
organise in the process itself, and all within a boundary of its own making.
(Bitbol and Luigi, 2004: 99).
Yet, another example of how metabolic exchange is viewed as an essential

component of life is provided by the Hungarian biologist Tibor Gánti ([1970]
2003). In the context of his Chemoton theory of minimal life, Gánti offers a list
of necessary conditions for life, what he calls ‘real (absolute) life criteria’.
Contending that a ‘living system has to perform metabolism’ (104), Gánti
unpacks this necessary criterion for life as follows:
By metabolism we understand the active or passive entrance of material and

energy into the system which transforms them by chemical processes into its
own internal constituents. Waste products are also produced, so that the chemical
reactions result in a regulated and controlled increase of the inner constituents as
well as in the energy supply of the system. (Gánti, [1970] 2003: 76)
Similar to Sagan’s standard metabolic definition, Gánti’s necessary (but not

sufficient) criterion emphasises the extraction of energy from the environment
into a bounded system that is then broken down (i.e., catabolism) and used to
construct the system’s component parts (i.e., anabolism) in a controlled and
regulated manner. And like Sagan’s standard definition, Gánti’s criterion is
explicit about the nature of the products of metabolic exchange (i.e., internal
constituents and waste products). Gánti’s criterion is, however, more akin to the
autopoetic definition of life in the sense that it emphasises the circular self-
production of the metabolising system. Interestingly, of all three accounts,
Gánti’s criterion is the only one which mentions the production of waste.
These three examples are representative of a more general and long-standing
view in biology that metabolic exchange is necessary for life.13 Moreover,
I would like to argue that these examples suggest that at least some biologists
assume life-living equivalence and the fact that at least some biologists assume
life-living equivalence is enough to motivate the development of the biotic
taxonomy that will follow (Section 3.3). How might this be the case? Take for
example Sagan’s description of a metabolic definition. That which is being
defined is life. This is evident given the title of the encyclopaedia entry is
‘Definitions of Life’. Sagan, however, then goes on to define what a living
system is. This switch from life to living is only justified against a background of
life-living equivalence. For answering the question ‘what is a living system?’ is
supposed to shed light on what life is.14
What about Bitbol and Luisi? At first blush, their interpretation of Maturana
and Varela seems innocent enough. Upon closer inspection, however, their use
of life-living equivalence surfaces. Bitbol and Luisi offer a definition of life, as
is evidenced by their writing ‘life is’, and then provide a metabolic definition.
So far, so good. However, Maturana and Varela’s autopoietic theory is focused
upon defining living systems. This is clear when they write:
[W]e shall first characterise the kind of machines that living systems are and
then show how peculiar properties of living systems may arise as
a consequence of the organisation of this kind of machines [sic]. (1973: 78)
and then:
An autopoietic machine is a machine organised (defined as a unity) as

a network of processes of production (transformation and destruction) of
13
The idea that life requires metabolism (and reproduction) goes at least as far back as Aristotle,
who is often considered the father of biology.
14
Although Sagan was an astronomer, not a biologist, I think it’s fair to say that his deployment of
life-living equivalence is representative of a general attitude adopted by many of the biologists
that he attributes his standard metabolic definition to.
components which: (i) through their interactions and transformations con-

tinuously regenerate and realise the network of processes (relations) that
produced them; and (ii) constitute it (the machine) as a concrete unity in
space in which they (the components) exist by specifying the topological
domain of its realization as such a network. (Maturana and Varela, 1973:
78–79)
Maturana and Varela are careful to focus upon living systems as their intended
objects of analysis and do not, as Bitbol and Luisi’s interpretation suggests,
equate definitions of living systems with definitions of life.15 Bitbol and Luisi’s
interpretation of Maturana and Varela’s autopoietic definition of living system
exemplifies life-living equivalence and how readily it is assumed even by the
likes of careful biologists and philosophers.
Gánti’s definition also assumes life-living equivalence. His real- (absolute)
life criteria turn out to be necessary and sufficient conditions for being a living
system. Metabolic exchange, a real- (absolute) life criterion, is something that
livings systems must perform.
If these examples are representative of a general acceptance and use of life-
living equivalence on the part of biologists and philosophers, then a problem
arises in the context of understanding the biotic status of dormant spores.16 For
anyone who assumes life-living equivalence takes metabolic exchange as
necessary for being living system is committed to an incoherent view if there
are metabolically inert examples of life.17 Dormant spores, as we have already
seen, are one such example that most biologists acknowledge as such. Let us
now turn to look at Physarum spores in particular, focusing on what makes
spores metabolically inert and why one might plausibly consider them to be an
example of life. Although Physarum spores differ in some respects from those
of bacteria, something that I will soon clarify in more detail, there are shared
physiological changes that underly spore dormancy across taxa. It is the
15
Interestingly, later in an article entitled On Defining Life, Varela (1994) presents a similar
definition for (minimal) living systems. Given his earlier work (1973) with Maturana, his use
of life-living equivalence comes as a surprise to me.
16
Let it be stressed that the use of life-living equivalence is by no means limited to the context of
metabolic definitions (or theories) of life. Its prevalence extends to all aspects of biological
theorising that looks to expound upon life and biotic processes (e.g., theories and definitions of
life based upon reproduction, thermodynamics, etc.). The argument that I present here is merely
one manner to motivate renouncing life-living equivalence. A more general motivation, as I hope
to show, comes from the potential usefulness and conceptual clarity of the biotic taxonomy that
I develop in Section 3.3.
17
This is not meant to suggest that any of those authors who are committed to metabolic definitions
expounded upon above do or do not acknowledge that there are metabolically inert systems that
are examples of life. I am merely stating that if any of them do acknowledge that there are
metabolically inert systems that are examples of life, then given their use of life-living equiva-
lence their position is incoherent.
presence of these commonalities which allow using an investigation into

Physarum spores as a manner of understanding the biotic status of spores as
they are found across all taxa.
3.2 Putting Metabolism on Temporary Hold

In order to understand the metabolically inert nature of dormant spores in
Physarum, it is necessary to understand the process of spore development.
Recall that during the process of sporulation, a starved plasmodial cell differ-
entiates into multiple fruiting bodies (Section 2.3). Within the apical end of each
fruiting body the cellular cytoplasm cleaves, after which meiotic recombination
leads to the development of mononucleate haploid spores. Spore cellularisation
is completed as a thick, resistant cell wall develops around each compartmen-
talised nucleus and its surrounding cytoplasm, forming individual spores within
the spore case. As they mature over the hours that follow, spores (and the spore
cases that surround them) undergo a process of desiccation. Such drying out
enables spores to be light enough to be easily dispersed by wind, and seeing as
they are reproductive units (cells), wide dispersal increases the progeny’s
(ameboflagellates) chance of survival by decreasing resource competition.
Desiccation is due to the spore cases being vertically suspended on stalks, and
thus, being distanced from the moist substrate and exposed to air flow. As each
spore dries out, it loses the majority of its water content and metabolism ceases.
Why does cell desiccation result in its metabolism coming to a grinding
halt? The answer, put in simple terms, is this: metabolism involves various
chemical reactions that can only occur within a medium of water (Wharton,
2003). So, when cellular water is depleted to 20 per cent or below of its
normal content, it is inferred that metabolism has ceased (Clegg, 1979). It is
under these physiological conditions that a spore becomes dormant and thus
metabolically inert.
This brings us to the next crucial question. Despite their being ametabolic,
why might desiccated spores be considered examples of life? A hint is provided
by Gánti, who describing the state of ametabolic entities writes:
A system suitable for the occurrence of the processes in question may be

either functioning or in a state which is not functioning but is capable of doing
so. When this system is in its functioning state it is said to be living; when it is
in its non-functioning but functionable state it is capable of living, but it is not
dead. ([1970] 2003: 75)
I believe one implicit reason why many biologists acknowledge dormant spores
to be forms of life – a reason made explicit here by Gánti – has to do with the
idea that they retain a capacity to engage in metabolic exchange. Let me take
a moment to unpack this idea and put some ‘biological meat’ on what might
seem at first to be an abstract concept.
Were most organisms to undergo desiccation, they would die in the process;
their cellular structure would be destroyed beyond repair due to protein denatur-
ation (i.e., altering the shape or conformity of the proteins and hence preventing
them from playing a role in the various metabolic and regulatory functions that
they typically underwrite). This is not the case, however, with spores. In fact,
desiccation allows spores to remain viable despite the cessation of metabolism
that desiccation brings about, a process generally referred to as ‘anhydrobiosis’.18
During anhydrobiosis in eukaryotic spores, it is thought that most cellular water is
replaced by a sugar (‘trehalose’) that protects the structure of proteins and
membranes from the destructive effects of water loss (Clegg, 2001; Rikkinen
et al., 2019).19
In an anhydrobiotic state, if all goes well, a spore retains its capacity to
engage in metabolic exchange despite being metabolically inert. If something
goes awry and the spore loses this capacity, it dies and hence fails to be an
example of life any longer. I think this is an important point. If we don’t
recognise a spore as alive, then we can’t make sense of the significance of its
structure being destroyed. We wouldn’t be able to see this as ‘death’, but just an
ordinary physical degradation.
Suppose a desiccated spore encounters environmental water (or a moist
surface) again, and the preserved intercellular structure and membrane are put
to work once more so that metabolic exchange resumes. When this happens,
a spore’s capacity to engage in metabolic exchange is utilised. To be sure, even
when not utilising its capacity to metabolise, a spore retains that capacity (much
in the same way that your capacity to breathe does not somehow vanish when
you begin to breathe again after having held your breath for some seconds).
Retaining the capacity (unutilised or utilised) to engage in metabolic exchange
qualifies spores as examples of life and the mechanism underwriting anhydro-
biosis describes how a dormant spore retains its capacity to metabolise despite
its being unutilised. The continued functioning of metabolic pathways, on the
other hand, is how a non-dormant spore retains its capacity for metabolising; the
capacity is retained by utilising that very capacity. Non-dead dogs, bees,
18
Although the term ‘anhydrobiosis’ was not coined until 1959 by Keilin, that an organism’s
metabolism could come to a reversible halt was discovered around 300 years earlier by Antony
van Leeuwenhoek whilst doing experiments with desiccated ‘animacules’ (rotifers) that he
obtained from his gutter. Other anhydrobiotic organisms include tardigrades, brine shrimp,
some nematodes, resurrection plants, and some bacteria.
19
The idea that water is replaced by trehalose during anhydrobiosis is known as the ‘water
replacement hypothesis’ and was proposed by James Clegg (1986).
evergreens, octopuses, humans, and bacteria, all undoubtable examples of life

in biology, share this capacity to engage in metabolic exchange.20
Zooming out for a moment: anhydrobiosis in Physarum is coupled to repro-
duction, and because of this, what survives when metabolism resumes (when
the spore utilises its capacity to engage in metabolic exchange after dormancy)
is not the plasmodium that sporulated. Again, the plasmodium (and the gener-
ation that it represents) terminates with the nuclear cellularisation of the fruiting
body. Instead, it a plasmodium’s progeny that survives via the spore stage of the
life cycle (Section 2.4). This may be contrasted to bacterial spores. In the case of
bacteria, the same organisational form that transforms into a spore hatches from
the spore after germination; the bacterium that emerges after germination is
a continuation of the bacterial cell generation that sporulated. In this sense,
bacterial spores are more akin to Physarum sclerotia and microcysts, all of
which represent reversible (and optional) dormant stages within their different
life cycles.
There may be an interesting sense, however, in which one can view spore
development in terms of a reversible transformation. This requires zooming in
again. A transformation from (1) a metabolising spore directly after nuclear
cellularisation to (2) a metabolically inert spore in an anhydrobiotic state and
then back again to a (3) metabolically active spore during germination.21 The
reason that I have suggested why spores are acknowledged as examples of life
turns upon this fine-grained picture. The capacity to engage in metabolic
exchange remains constant throughout this transformation although that cap-
acity is only utilised in steps (1) and (3). It is in this sense that one might say that
the spore stage represents an irreversible transition in the life cycle of an
acellular slime mould, and it also represents a reversible metabolic transition
in spore development. Being able to separate these fine-grained (i.e., spore
development) and coarse-grained (i.e., Physarum’s life cycle) views is import-
ant because they provide two different informative perspectives to consider and
compare when analysing spores. Remaining aware of these two different
perspectives when focusing upon Physarum should make this quite apparent.
Having articulated one shared quality of life – one that I suspect lies at the
heart of at least some biologists’ intuitions that dormant spores qualify as life –
I would now like to put it to use in formulating a way of resolving the tension
that was articulated in Section 3. Recall that this tension arises when one,
20
Any of these organisms when dead, rather than representing an example of life, represent an
example of a biomarker – a sign of life that once existed.
21
See Segev et al. (2012) for evidence that entry into dormancy lasts several days for bacteria
B. subtilis. This spore development period in B. subtilis would be analogous to what I have
labelled period (1) in the development of Physarum spores.
assuming life-living equivalence, holds onto the idea that metabolic exchange is
necessary for being a living system and yet acknowledges that biologists regard
spores as an example of life. The way of resolving this tension that I will now
pursue involves jettisoning life-living equivalence and developing a taxonomy
around a distinction proposed by Lane (2016).
3.3 Being Alive versus Living

Molecular biologist Nick Lane, in his book The Vital Question, examines why
eukaryotes and the kind of traits that are characteristic to them (i.e., nuclei,
organelles, sex, and phagocytosis) have only evolved once from a single
prokaryotic predecessor in the four billon years that prokaryotes have existed
on Earth. In approaching this question, Lane asks a more fundamental one: what
is living? He considers what metabolically inert entities such as dormant spores
can suggest about life given that they are ‘completely stable in their non-living
state’ (2016: 55) and in doing so, he writes something rather revealing:
That [remaining stable in a non-living state] tells us something about the

difference between life and living. Spores are not technically living, even
though most biologists would classify them as alive, because they retain
a potential to revive. They can go back to living so they are not dead. (Lane,
2016: 55; my addition).
Lane, referring to dormant spores, distinguishes between life and living and, as
such, does not assume what I have been calling life-living equivalence. He does,
however, as I read him, suggest that being alive is necessary and sufficient for life,
what might be called ‘life-alive equivalence’. Importantly, he suggests that
retaining a potential to revive – to go back to living – is necessary for being
alive. In order to make sense of this condition, we must first have an idea of what
living is since being alive is characterised relative to living. In elucidating what he
takes to be the difference between life (being alive) and living, Lane writes:
Life is about structure (dictated in part by genes and evolution) but living –
growing and proliferating – is as much about the environment, how structure
and environment interrelate. (2016: 55)
Lane’s characterisation of the difference between life and living in terms of

structure and structure–environment interrelations may be plausibly viewed as
providing rough explanations of the two different ways that an entity can retain
a capacity to metabolise. More precisely, having the right structure explains
how the capacity to engage in metabolic change is retained without utilising it.
On the other hand, having the right structure and that structure’s having the right
ongoing interrelation with the environment explains how the capacity to engage
in metabolic exchange is both retained and utilised. To see this, consider that
a dormant spore is alive because its structure has been preserved in an anhy-
drobiotic state, allowing it to retain its capacity to engage in metabolism; yet
a dormant spore fails to be a living entity since that capacity is not being utilised.
On the other hand, a germinating spore – one that has encountered favourable
environmental conditions – is both alive and living. It utilises its capacity to
engage in metabolic exchange, and also retains that capacity in virtue of its
structure. This is also true of the pre-dormant spore. Lane’s distinction between
being alive and living thus lends support to the idea articulated above that
dormant spores are acknowledged to be life because they retain the capacity
to engage in metabolic exchange. Lane fleshes this idea out with the notion of
preserved structure.
Assuming that this analysis is correct, living can be viewed as something that is
additional to being alive – it requires more than just having the right structure. To
understand how living builds upon being alive and yet both categories remain
distinct, consider the fact that being a member of the species P. polycephalum is
distinct from being a member of the genus Physarum (see Table 1). That this is the
case is compatible with the fact that being a P. polycephalum is a specific way of
being a Physarum. This kind of relation is often described by philosophers in
terms of being a ‘specification relation’, ‘where the more specific property can be
understood as a conjunction of the less specific property and some independent
property or properties’ (Wilson, 2023: 1). Living may be viewed as a species of
the genus being alive in the same way that P. polycephalum is a species of the
genus Physarum. This has the result that any entity that is living is also alive
(having the right structure and having the right interrelation with the environment
so as to utilise that structure), although there may be entities that are alive which
simultaneously fail to be living (only possessing the right structure). It is in this
way that living builds upon being alive – it is a way of being alive.
Lane, in the passage above, also describes living in terms of ‘growing and
proliferating’. Whether he sees growing and proliferation (i.e., reproduction) as
contingent features or necessary features of living is not clear. I would like to
argue that although vegetative growth and repair – protein synthesis – is part and
parcel of utilised metabolism (anabolism) and hence living, there is a reason to
view proliferation as a contingent feature of living systems. For example,
a metabolising and hence living Physarum spore is not a reproducing entity but
a reproductive cell that develops under suitable conditions into a reproducing
entity. In this sense, a non-dormant spore is similar to a metabolising sperm cell or
egg cell, none of which proliferate. Although non-dormant spores cannot repro-
duce, protein synthesis occurs until a spore enters dormancy (Sauer et al., 1969)
and again during germination. One general take home from this example is that
being a living system and being a proliferating system can come apart, although in
many cases they do not.
3.4 Dead, Structura Vivens, or Living: A Taxonomy

With these conceptual distinctions to hand, I would like to suggest that the biotic
status of Physarum spores can fall into one of three possible categories: dead,
‘structura vivens’, – which literally translates from Latin into ‘living structure’ –
or, living (henceforth referred to as the ‘DSVL taxonomy’). The last two states
constitute the domain of life. Dormant spores fall into the category of structura
vivens; they are entities that are alive and with the right structure for living yet
they are not living. Pre-dormant and germinating spores fall in the category of
living and hence also alive. Spores that have lost their capacity to engage in
metabolic exchange fall into the category of dead (i.e., lifeless) and are thus
neither living nor alive (see Figure 3). There are no sharp cut-offs that exist
between these categories given that both retaining the capacity to metabolise
and utilising a retained capacity to metabolise are dependent on biological
processes (e.g., intracellular replacement of water with trehalose) that are
graded. Even dying takes time, whether it occurs via ageing or more rapidly
Figure 3 Dead, alive, or living (DAL) taxonomy – conceptual space: life

refers to being alive or both being alive and living; living is a way of being alive.
Dead excludes any instance of life and as such excludes both being alive and
living. Being alive excludes being dead. Any living entity is also alive but some
entities that are alive are not living. Although I have represented these
categories as being sharp, something that is useful for the sake of explication,
I take it that there are no sharp cut-offs that exist between any
of these categories.
as a result of injury. Since the biological processes that give rise to the separ-
ation of the categories structura vivens, living, and dead are not discrete, these
categories are themselves rendered fuzzy – exemplifying the kind of fuzzy
boundaries that are typical in the biological world.
The focus of this section thus far has largely been two of the three biotic states
which I have argued apply to Physarum spores (structura vivens and living).
A third biotic state, dead, which I have given less attention is, however, no less
important. When we think of death, we tend to intuitively think of irreversibly
passing from a state of living to one devoid of life altogether. This is an
oversimplification of a complex picture that is largely due to the fact that our
intuitions are based upon what we know best – human life – and this is not
representative of all life.
Different ways of influencing environmental selection effects that have evolved
over time, and resulted in stage-specific phenotypes within a life cycle, have also
opened up different ways that life can cease to be. Currently, it is thought that in the
acellular slime moulds (myxomycetes), the ameboflagellate stage was ancestral to
the plasmodial life cycle stage (Collins, 1979). Alone this would suggest not only
that sexual reproduction is an evolved trait in the acellular slime moulds but,
crucially, that sclerotisation and sporulation (see Section 2) evolved from a life
cycle that consisted exclusively of asexually reproducing ameboflagellates. Let this
sink in for a minute. The ability to decouple being alive from living evolved at least
two separate times in the acellular slime moulds (myxomycetes) with the evolution
of the sclerotia and the reproductive spore (and possibly a third with the microcyst).
The evolution of these different life cycle stages resulted in not only new ways to
meet selection pressures head-on but also new ways to die.
For Physarum, death can occur from not only from a state of living but also
from a state being alive. When a Physarum dies from a state of living, it dies
from a state of either being an ameboflagellate, a plasmodium, a reviving
sclerotium, a young fruiting body, an immature spore, or a germinating spore.
When a Physarum dies from a state of structura vivens, it dies whilst either
being a sclerotium, a microcyst, or a dormant spore. Let us now take a moment
to consider how a spore might die.
Given that being alive is about preserving structure (Lane, 2016), one way for
a spore to die is for it to somehow lose its life-bearing structure and, as a result,
irreversibly lose its capacity to engage in metabolic exchange. This degradation
may occur across a wide range of rates. At one extreme, a spore can suffer
significant structural damage instantaneously to such a degree that the capacity
to metabolise is altogether thwarted; at the other extreme it may suffer structural
deterioration over time such that the capacity to metabolise becomes increas-
ingly limited and is slowly lost. Both are changes to the structural integrity of
the spore. The most vivid examples of the former extreme of structural damage
are a spore’s being destroyed by being crushed or digested. The latter extreme of
structural deterioration is spore ageing, something that is measured by the
reduced rate of germination (Smith and Robinson, 1975; Segev et al.,
2012).22 Either significant structural damage or structural deterioration over
time and their accompanying DNA damage and/or protein modification may
render a spore dead. This covers all three possible categories of the DSVL
taxonomy that biotic status of Physarum spores may fall into.
The DSVL taxonomy may be distinguished from the taxonomy elucidated by
Clegg (2001) and Wharton (2003), both of whom contend that biological organ-
isation may be classified in terms of three different biotic states: alive, dead, and
cryptobiotic. As I understand their taxonomy, ‘alive’ refers to being metabolically
active, whilst ‘cryptobiotic’ refers the state of metabolic standstill occurring in
response to various physical stresses, including desiccation (anhydrobiosis),
freezing (cryptobiosis), and osmotic stress (osmobiosis) (Keilin, 1959).
However, by conceptualising the difference between being structura vivens and
living in terms of retaining a capacity to metabolise and utilising that retained
capacity, the DSVL taxonomy offers the advantage over Clegg and Wharton’s
taxonomy of being able to capture the specification relation between being alive
and living. As conceptualised by Clegg and Wharton, the notion of ‘alive’
(metabolically active) cannot coherently be a specific way of being cryptobiotic
(metabolically inactive). This is undesirable because when answering a question
like ‘what makes a dormant spore a form a life?’ (or equally ‘what makes
a dormant spore alive?’) one of the things that biologists presumably would
like to do is identify the shared feature(s) of dormant and non-dormant spores.
The DSVL taxonomy, in capturing the specification relation between alive and
living captures at least one such feature: dormant and non-dormant spores both
retain the capacity to engage in metabolic exchange via their preserved structure.
Entering into an anhydrobiotic state is how spore structure is preserved and how
ametabolic dormant spores remain alive like non-dormant spores.
3.4.1 Generalising the DSVL Taxonomy

The DSVL taxonomy provides a clear manner for thinking about the biotic
status of Physarum spores and those of other spore-producing taxa over the
22
Instantaneous damage suffered by a spore may also not be severe enough for it to result in
immediate death; rather, such damage may only be fatal after an organism begins to utilise its
capacity to metabolise again. A telling case of this type is provided by Wharton (2003), who
describes Hinton’s (1960) observation of an anhydrobiotic larva of the midge P. vanderplanki.
The larva, after suffering damage during its dormancy, revived only to die as a result of that
damage.
course of spore development (the zoomed-in perspective). This is because of the

common structural and physiological features that are shared by all spores. The
DSVL taxonomy can also be used to understand how each stage occurring
within a life cycle or when dead is related to others in virtue of their shared
biotic status (the zoomed-out perspective).
What is the scientific value of recognising these shared biotic relations? To
take an example using stages of Physarum’s life cycle: dormant spores are
analogous to sclerotia and microcysts in being non-living entities that are
nevertheless alive; they are entities with the right structure for living and
hence alive and yet they are not living; they are structura vivens. Grouping
the entities of these respective stages as structura vivens prompts us to ask
questions about the different underlying mechanisms allowing such entities to
remain alive without utilising their capacity to engage in metabolism. The
replacement of water with trehalose during anhydrobiosis is one – but most
likely not the only – mechanism underwriting the retained capacity of dormant
spores to metabolise, but it remains an open question as to whether the same
mechanism of water replacement is (at least partly) responsible for how both
sclerotia and microcysts remain alive.
Importantly, in recognising these entities as having the same biotic status it is
natural to pose questions regarding the differences and/or similarities between
their structure preserving mechanisms. If both plasmodia and spore-producing
fruiting bodies were evolutionary additions to an ancestral ameboflagellate life
cycle (Collins, 1979), then we might expect that the mechanisms underwriting
the structural preservation of dormant spores and sclerotia built off of those that
allowed microcysts to remain structura vivens. That is, early structure preserv-
ing mechanisms in dormant microcysts may have laid the ground for further
evolutionary innovation, resulting in two additional manners of decoupling
being alive from living in the complexifying life cycle of acellular slime
moulds. Whether or not this is the case is a question to be scientifically pursued.
To be clear, I am not saying that questions about the mechanisms underlying
dormancy cannot be posed or approached without the DSVL Taxonomy. They
can and have (Clegg, 2001; Wharton, 2003). Rather, my claim is simply that the
conceptual distinctions of the DSVL taxonomy make these kinds of questions
easier to formulate and help them to remain contextualised within the larger
domain of inquiry – life; a domain that includes both dormant entities and
metabolising entities alike.
Another way of generalising the DSVL taxonomy is to use it to compare the
biotic status of various life cycle stages of different taxa. Such a comparison
prompts interesting questions constrained by the concepts of ‘dead’, ‘structura
vivens’, and ‘living’ and the relations amongst them. For instance, we may
compare the biotic status of the stages making up the life cycle of the bacterium
Bacillus subtilis with those of Physarum. Upon identifying the stages in which
B. subtilis is structura vivens (i.e., dormant), the question of how B. subtilis
spores preserve their structure and whether those structure preserving mechan-
isms are similar to those underwriting spores, sclerotia, and/or microcysts in
Physarum can be posed (assuming that the mechanisms underwriting structural
preservation in the latter three stages differ to some degree). Examples of how
the DSVL taxonomy applies to spores across taxa, to each of the organisational
forms making up Physarum’s complex life cycle, and to organisational forms of
Bacillus is provided in Figure 4(a–d).
It should be clear that while the conceptual distinctions of the DSVL tax-
onomy are conducive towards thinking about the biotic status of spores, the uses
of the taxonomy are by no means limited to thinking about spores. It can be
applied to any organism but will provide the most insightful perspective on
those organisms which have evolved a capacity to decouple being alive from
Figure 4 (a–d)
living. For example, tardigrades do not form dormant spores; however, they can
enter into various reversable dormant states and remain alive by balling up and
forming a resistant ‘tun’ during unfavourable conditions (Møbjerg and Cardoso
Neves, 2021) (Figure 4d). Although water replacement with trehalose may be
a common feature between dormant spores and dormant anhydrobiotic tuns
(Wharton, 2003), deploying the DSVL taxonomy prompts us to ask whether the
transition back to the state of living for both desiccated spores (i.e., spore
germination) and desiccated tuns (i.e., tun reviving) are similar processes.
This highlights that there are at least two explananda (phenomena to be
explained) when it comes to the developmental transitions that take place across
the domain of life: how some living entity transitions to being structura vivens
and how that entity goes back to living again.
3.5 Spore Ageing

When comparing different taxa that have evolved the capacity to decouple being
alive from living, one thing that becomes apparent is that some of them can
remain alive in an ametabolic state longer than others. One recent finding
suggesting a species of nematode has been revived after 46,000 years of anhy-
drobiotic dormancy in the Siberian permafrost (see Shatilovich et al., 2023).23
Narrowing the focus once again to spores: dormant bacterial spores have been
revived after being trapped in amber for twenty-five to forty million years (Cano
and Borucki 1995). Dormant Physarum spores have a considerably shorter period
of several years after which they can be revived (Clark and Haskins, 2016).
Despite these differences, one thing which all dormant spores (and more gener-
ally all dormant entities) have in common is that how long they can remain alive is
limited. There is an interesting mirroring of the phenomenon of spore ageing and
the kind of ageing that living entities undergo that the distinctions between
structura vivens, living, and dead allow us to think about (see Figure 5).
Figure 5 A mirroring of spore ageing and senescence in vegetative cells. The

colour version of this figure is available at www.cambridge.org/Sims
23
This assumes that the samples found were not contaminated.
A dormant spore’s potential to metabolise changes over time and as such, spore
ageing can be viewed as a decreasing capacity to metabolise. Spore death, on the
other hand, is the complete loss of the capacity to metabolise. ‘Senescence’, ageing
that is experienced exclusively by living entities, is characterised as the time-related
loss of cellular growth, repair, and reproductive functions (Gilbert, 2000). Casting
this loss of cellular function as a decreasing capacity to engage in metabolic
exchange on the part of a living system, when living is conceptualised as a way
of being alive, investigating spore ageing (and eventual spore death) may be
a valuable proxy method for gaining insights into senescence. Setting aside the
fact that different organisms have different senescence mechanisms (Bodnar,
2014), the question arises as to whether senescence may be underwritten by
some of the same irreversible structural changes as spore ageing. For example, is
cellular senescence accompanied by the same or similar kinds of protein structure
modifying degradation that accompanies modification of protein structure in ageing
spores? Another question is whether the same kinds of environmental factors that
affect the progression of spore ageing might also affect the progression of senes-
cence. In terms of practical implications, the possibility of using spore ageing in
Physarum (or other spore bearing organisms) as an easy-to-study model system/
phenomenon to investigate fundamental aspects of senescence in other taxa may
very well be where the rubber meets the biological road. The DSVL taxonomy
furnishes the conceptual distinctions to investigate this possibility.
Having made a case for how one particular stage of Physarum’s complex life
cycles (the spore) can be used as a starting point for thinking about the biotic
status of spores more generally, let us now turn to another stage, the plasmo-
dium, and a challenge that its fascinating behaviour poses for the notion of
biological individuality.
4 Biological Individuals: A Puzzle Concerning Plasmodial

Fragmenting and Fusing
When answering the question ‘what is a biological individual?’, one is faced
with the task of providing an account of what in the biological world ‘consti-
tutes a countable, relatively well-delineated, and cohesive unit’ (Pradeu, 2016:
762). Whether it was Charles Darwin’s ([1839] 1967) concern about how to
delineate barnacles and whale ‘compounds’ living in close association, Thomas
Huxley’s ([1859] 2008) befuddlement regarding coral polyp individuation, or
Daniel Janzen’s (1977) puzzlement over individuating clonally reproducing
dandelions and aphids, it is clear that this question has perplexed biologists
for (at least) nearly two centuries. Today, biological individuality continues to
be a topic of joint interest to both biologists and philosophers of biology.
Various ways of addressing biological individuality have been developed in

response to concerns, amongst other things, about how to distinguish specific
cases of growth from reproduction and/or when a group of individuals no longer
counts as a mere group but can be construed as an individual in its own right.
Many times, such concerns have been motivated by puzzling cases from the
biological world that challenge our folk intuitions about biological individual-
ity. Are runner strawberry plants that are produced by and still connected to
a main strawberry plant each individual’s or are they distributed parts of the
main plant? In addition to each member of a honeybee colony being an
individual, is the colony itself an individual? In this tradition, here is a novel
puzzle involving the behaviour of P. polycephalum.
A first observation: during Physarum’s vegetative plasmodial stage (i.e., when
they appear as a bright yellow mass of protoplasm), they have been observed to
sometimes fragment into two separate, autonomous plasmodial cells. This hap-
pens, for example, when there are two spatially distanced food sources in a Petri
dish and a single plasmodium fragments after reaching both (Nakagaki et al.,
2000, 2001). A second observation: complete fusion of separate plasmodial cells
has been observed to typically occur when plasmodia are closely related genetic-
ally, phenotypically identical (Clark and Haskins, 2012; Vogel and Dussutour,
2016), or, more generally, when they come from the same strain (Grey, 1945).
Putting these two observations together, the possibility of an interesting conjunc-
tion of behavioural patterns arises.
Since both fragmentation and fusion are individually part of Physarum
plasmodia’s behavioural repertoire, there is little reason to think that fragmen-
tation followed by fusion would not occur given the combination of experi-
mental conditions that originally elicited fragmentation and fusion (e.g.,
a Petri dish of a certain size, the placement of food at different locations,
and then wait for fusion to occur after food consumption). That said, the
possibility of fragmentation followed by non-fusion cannot be completely
ruled out either. Given that such a combined experiment, as far as I know, has
yet to be performed, the possibility should be left open that fragmentation may
be followed by non-fusion sometimes. Focusing on the plasmodial cell dyad –
fragment pieces that we would expect to usually fuse but sometimes do not –
a pressing question arises: is there any plausible reason to view the two
spatially non-contiguous plasmodial cells as jointly constituting a biological
individual in its own right?
The importance of various accounts and notions of biological individuality is
heavily tied to different biological subdisciplines, their aims of inquiry, and
respective methodological practices (Lidgard and Nyhart, 2017; Love and
Brigandt, 2017). Different notions of individuality lead to different ways of
counting the things that feature into the explanations of phenomena of interest.
Addressing the question of whether the two plasmodial cells in the described
combined experimental scenario jointly constitute a biological individual is
grounded in myxomycete biology and may indeed be of value to this subdisci-
pline (or microbiology more generally). This value may lie in arriving at a more
precise understanding of the kinds of behaviour that a single Physarum plasmo-
dium is capable of in controlled laboratory settings. Admittedly, it is not telling
of what a plasmodium does in its natural habitat. Another value may lie in
something as fundamental as understanding when plasmodial fragmentation
sometimes counts as reproduction and when it does not. Lastly, since the
question is based upon an assumption about what would be likely to occur if
two experiments were combined, it may prompt those interested biologists to
investigate fragmentation and fusion patterns in the lab. This is a case in which
the posing of a question about biological individuality may itself have some
potential value to biology regardless of how it is answered.
In what follows, two different concepts of biological individual will be
brought to bear on the question of whether the two plasmodial cell fragments
in the described scenario jointly constitute a biological individual with the hope
of gleaning some insight into plasmodial individuality. The respective concepts
are those associated with what has been called Darwinian individuals and
metabolic individuals (Godfrey-Smith, 2013a).24 I will argue that the plasmo-
dial dyad fails to qualify as a single Darwinian individual. On the other hand,
taking fragmentation and fusion patterns into account may indeed warrant
viewing the dyad as having some degree of metabolic individuality. This,
however, requires expanding the ‘orthodox’ view of metabolic individuality
in a way that does justice to the remarkable morphological and behavioural
plasticity exhibited by a plasmodium.
This section will be organised as follows: firstly, I will describe the details of
both Darwinian individuality and metabolic individuality. Using these notions
of individuality, I will then evaluate the plasmodial dyad arriving at negative
conclusion regarding its status as a Darwinian individuality. I shall then evaluate
the dyad in terms of metabolic individuality, taking into account the larger
behavioural context of fragmentation and fusion or non-fusion. After introdu-
cing a simple diagrammatic schema of plasmodial fragmentation-fusion and
fragmentation-non-fusion patterns, I will argue that the possibility of the first of
24
To be sure, Godfrey-Smith (2013a, 2013b) formulates an account of ‘organisms’ that is based
upon the process of metabolism. To avoid any unnecessary confusion that might arise in adopting
his specific use of the term, given how widely a more general notion of organism is used in this
Element, in what follows I will continue to use ‘metabolic individuals’ to refer to Godfrey-
Smith’s ‘organisms’.
these patterns happening at all requires rethinking the orthodox concept of

metabolic individuality. Such a conceptual revision should reflect the fact that
both fragmentation and fusion are metabolically beneficial behaviours. Given
that fusion after fragmentation rules out reproduction by definition, the most
parsimonious view is that there is one persisting, spatially oscillating metabolic
individual across both fragmentation and fusion events. Lastly, I will articulate
a counterfactual analysis of metabolic individuality specific to such cases of
fragmentation and fusion in plasmodia or other organisms that possibly share
this striking behavioural capacity.
4.1 Two Kinds of Biological Individual

In this section, I will review the notions of Darwinian individuality and metabolic
individuality as developed and formulated by Godfrey-Smith (2009, 2013a).25
I will focus upon these two specific types of biological individuals because they
offer two very different individuality concepts that can be used to approach the
puzzle of plasmodial fragmentation and fusion.26
4.1.1 Darwinian Individuals

Godfrey-Smith, in his seminal book Darwinian Populations and Natural
Selection (2009) and in a series of papers published afterwards, develops one
evolutionary notion of biological individuality that he calls ‘Darwinian individ-
uals’. According to Godfrey-Smith, Darwinian individuals are reproducing
entities that are capable of forming parent–offspring lineages upon which natural
selection can act. To unpack this notion, Godfrey-Smith uses a general definition
of evolution by natural selection provided by Lewontin (1985). Accordingly,
natural selection occurs whenever there is phenotypic variation, heritability of
that variation from parent to offspring, and differential reproductive success.
Thus, failing the capacity to reproduce and pass on variation means, an entity
(or collective of entities) falls short of being a Darwinian individual in any sense.
Given the centrality of evolutionary theorising and evolutionary modelling
in biology, the notion of Darwinian individuality is one that plays – at least
implicitly – an important role therein (Clark, 2011; Lidgard and Nyhart, 2017).
For example, being able to measure differential reproductive success and, hence,
to predict how a phenotype might spread throughout a population requires being
25
There have been numerous ways that the notion of biological individuality has been developed
by both biologists and philosophers. For many such examples, see both (Clark, 2010) and
(Lidgard and Nyhart, 2017).
26
For a different analysis biological individuality that considers Physarum’s ability to fuse after
being split into different smaller individuals, see (Smith-Ferguson and Beekman, 2019).
able to count differences in the number of offspring produced by a parent/parents.

Doing this presupposes an ability on the part of the counter to be able to
distinguish both individuals that reproduce and offspring from parts of individ-
uals that have resulted from mere growth (e.g., leaves of a plant) and groups of
independently reproducing individuals (e.g., a school of fish or a field of dande-
lions). The notion of a Darwinian individual is meant to capture the appropriate
countable unit of reproduction upon which evolution by natural selection acts.
Darwinian individuals sometimes (but not always) map onto those individuals
that are most easily discerned by us, those individuals – typically metazoans – that
populate our folk biology (e.g., individual dogs, birds, humans, bees, etc.). That
said, because there are many different kinds of reproducing, lineage forming
entities, the notion of a Darwinian individual also applies to viruses, genes,
chromosomes, and some collective entities (Godfrey-Smith, 2013a).
Recognising that modes of reproduction and reproducing units are both prod-
ucts of evolution and also how evolution occurs, Godfrey-Smith identifies three
different types of reproducer. The first type, which he calls a ‘scaffolded reprodu-
cer’, is one that fails to have its own reproductive machinery and hence requires
another system to reproduce itself. Viruses and genes are two examples.
The second, a ‘simple reproducer’, is a Darwinian individual that can reproduce
through its own resources and does not contain other reproducers like itself as
component parts; that is, a simple reproducer does not contain other reproducers
that are not themselves scaffolded reproducers. A paradigmatic example of
a simple reproducer, he suggests, is a bacterium. A third type of reproducer is
a ‘collective reproducer’. Godfrey-Smith characterises such a reproducer as one
that (non-exclusively) contains other reproducers of any of the three categories as
constituent parts at lower levels of its organisational hierarchy.27 We Homo
sapiens and other multicellular organisms are collective reproducers since we
are composed of reproducing bodily (‘somatic’) cells, but honeybee colonies are
also collective reproducers to some degree (as will be soon explained).
Darwinian individuality has a gradient nature – an entity can be more or less
of a Darwinian individual than another. A colony of honeybees qualifies as
a Darwinian individual but less so than, say, a bird or a human. In the case of
collective reproducers, Godfrey-Smith fleshes the graded nature of Darwinian
individuality out in terms of the degree to which a collective’s mode of
reproduction exhibits three features: ‘germlines’, ‘reproductive bottlenecks’,
and ‘integration’. Whereas scoring high across all three features is characteristic
of paradigmatic collectively reproducing Darwinian individuals, a low score
27
Godfrey-Smith acknowledges the possibility of collective reproducers being made up of other
collective reproducers, but rejects the idea that there can be collective reproducers ‘all the way
down’ (2009: 88)
across all three features suggests the presence of a mere group. Darwinian
individuals can fall anywhere in between these high or marginal scores. Let
me briefly unpack each of these features in turn.
Germline refers to the presence of a division of reproductive labour amongst
the different entities in a collective. Germ cells in mammals, for example, are the
only cells from which the same kind of organism can be reproductively derived.
Mammalian somatic cells, on the other hand, can reproductively give rise to only
differentiated cells like themselves and not an entire organism. A colony of honey
bees also has a certain degree of reproductive specialisation, their different castes
functioning analogously to germ and soma cells in mammals in important ways.
Reproduction of the colony is limited to queens and male drones, whereas female
workers are functionally sterile. A division of reproductive labour is a mechanism
that ensures that selection occurs at the level of the collective individual (e.g., the
individual human or honeybee colony) as opposed to independent selection
occurring also at the level of its nested parts (e.g., somatic cells or the individual
honeybee); it de-Darwinises lower-level units (Godfrey-Smith, 2009).
Godfrey-Smith characterises a reproductive bottleneck as a narrowing that
marks the start of a new generation in a life cycle, something that often takes
the form of a single cell. Bottlenecks serve as a mechanism to introduce variation
into the next generation given that small genetic changes in a single cell can result
in significant downstream effects over the course of development. Like germ-
lines, bottlenecks are a matter of degree. Lastly, integration refers to a more
general kind of division of labour that is characteristically exhibited to greater or
lesser degrees by collective reproducers. It is a division of labour other than that of
a reproductive division of labour. For instance, integration may take the form of
‘the mutual dependence of parts, and the maintenance of a boundary between
a collective and what is outside it’ (Godfrey-Smith, 2013a: 21). Interestingly,
Godfrey-Smith (2013a) sees behaviour-coordinating chemical communication
and waggle dances that occur between honeybees as counting towards the colony
having some degree of integration, suggesting that spatial contiguity is only one
manner of being integrated (also see Herron, 2017).
Germlines, bottlenecks, and integration are features of one kind of Darwinian
individual – a collective reproducer. Both simple and scaffolded reproducers
represent other kinds of Darwinian individuals that, like collective reproducers,
speak of degrees of Darwinian individuality.
4.1.2 Metabolic Individuals

Another way that biological individuals have been conceptualised is not teth-
ered to evolutionary theory or reproduction; rather, it is physiology (i.e., the
study of the various mechanisms that allow biological systems to maintain

themselves despite fluctuation in environmental conditions) that biological
individuality is tied to. Metabolic integration is one way that physiological
individuality has been fleshed out historically (J. Huxley, [1912] 2022) and
continues to be a central concept for approaching difficult questions regarding
biological individuality.28 One such question is concerned with ‘mutualist
symbiotic associations’ – an association of two or more heterospecific organ-
isms that each benefit from their reciprocal interactions. For example, Vibrio
fischeri bacteria colonise the internal cavity of the Bobtail squid (Euprymna
scolopes), feeding upon mucus produced by the squid. In turn, as the density of
the bacterial colony grows, V. fischeri begin to luminesce as a result of quorum
sensing, allowing the glowing and shadowless squid to hunt undetected by
predators or prey. At dawn, the squid expels most bacteria. As it rests over
the day, the remaining colony repopulate its cavity, and the cycle begins anew.29
Does such a squid–bacterial association count as a metabolic individual – if only
a temporary one – in its own right? Answering such a question seems important
if not for the fact that symbiotic associations are ubiquitous in nature – one of
which includes us and our various gut bacteria (Dupre and O’Malley, 2009;
Gilbert et al., 2018), but also because symbiosis is thought to have played
a central role in the evolutionary transition from prokaryotes to eukaryotes
(Maynard-Smith and Szathmary, 1995).
It is now generally acknowledged that the prokaryote–eukaryote transition
resulted from a prokaryote cell (an archaeon) engulfing another (a bacterium)
and, rather than consuming it, the host cell benefited from the engulfed cell’s
metabolic by-products and simultaneously provided a stable environment for
the engulfed cell to maintain itself over time.30 The mutual metabolic integra-
tion of both the engulfed cell and the host cell provides a plausible explanation
as to how the tight interaction between two (Darwinian) individuals may have
resulted in the evolution of a new kind of (Darwinian) individual – a new unit of
selection. Thus, the formation of a metabolic individual (e.g., an endosymbiont
bacterium and its host archaeon) was a precursory stage on the way to a new unit
of reproduction (i.e., a eukaryote). Although metabolic individuality is not
28
See (Pradeu, 2016) for another manner of fleshing out physiology-based biological individuality
in terms of immune tolerance.
29
For a comprehensive overview of Bobtail squid and V. fischeri symbiosis, see (McFall-Ngai,
2014).
30
This is a general description of endosymbiotic theory, the renewed interest of which in evolu-
tionary biology can be accredited to Lynn Sagan (1967) – thereafter known as Lynn Margulis.
Today, it is accepted by most biologists that cellular mitochondria (the ‘metabolic powerhouses’
found within all eukaryotic cells) are derived from an ancient endosymbiotic event in which
a bacterium was engulfed by archaeon cell giving rise to an ancestral eukaryote. See Martin et al.
(2015) for further details about the endosymbiotic origins of eukaryotes.
tethered to evolutionary theory, it provides one valuable way of thinking about

how certain new types of Darwinian individuals came (and perhaps continue to
come) into being. So, what is a metabolic individual?
Let us begin by focusing on what they are not. Metabolic individuals needn’t
(but can) be the kinds of things that reproduce; in contrast to Darwinian
individuals, reproduction is only a contingent feature (Godfrey-Smith, 2009).
One result of this is that metabolic individuals can have any evolutionary
history, something that opens up a theoretical space to consider how metabolic-
ally integrated entities that cannot form parent–offspring lineages together
can nevertheless qualify as more than a mere collection of independent entities.
This is one reason why metabolic individuals can potentially play a role in
understanding how some new Darwinian individuals could have emerged in the
first place (e.g., unicellular eukaryotes with their endosymbiont mitochondria).
Now, to positive characterisation: according to Godfrey-Smith, metabolic
individuals are
systems comprised of diverse parts which work together to maintain the

system’s structure, despite turnover of material, by making use of sources
of energy and other resources from their environment. (2013a: 25)
According to this view – what I shall continue to refer to as the ‘orthodox

view’ – metabolic individuals are systems made up of heterogeneous parts, the
nature of which allows for some kind of functional (metabolic) integration to
arise between them. Having diverse parts amounts to systems possessing different
features and capacities (e.g., morphology, biochemical responses, behaviours,
etc.) that constrain mutually supportive metabolic interaction. Thus, we can think
of the parts of a metabolic individual as exhibiting a division of metabolic labour
(e.g., the V. fischeri luminesce and contribute to the bobtailed squid’s biolumines-
cent camouflage, whilst the squid provides mucus food and a reproduction
conducive environment for the bacteria).
Importantly, the orthodox view emphasises that the diverse parts of a metabolic
individual must function together in the service of maintaining the individual.
That is, such individuals ‘are essentially persisters, systems that use energy to
resist the forces of decay, and only contingently things that reproduce’ (Godfrey-
Smith, 2013a: 25). One way that a metabolic individual is maintained, according
to Godfrey-Smith, is in virtue of cooperation between its parts (see also Queller
and Strassman, 2009). I think it is fair to interpret Godfrey-Smith as viewing
cooperation as a specification of the type of metabolism-relevant integration that
occurs between the parts of a metabolic individual that contribute to its persist-
ence. Since such cooperation is a matter of degree, metabolic individuality is itself
a gradient notion (Godfrey-Smith, 2009). Without more than a marginal degree of
metabolism-relevant integration, a collection of entities is no more than a group of

spatially localised members. Such integration is illustrated in the case of the
bobtail-V. fischeri- mutualistic symbiosis, where the squid–bacteria association is
maintained nightly as a camouflaged, hunting unit in virtue of the activities of
both symbionts.
Cooperation via metabolic division of labour places no demand on metabolic
individuality with respect to spatial contiguity. As long as the parts of
a collection are interactively organised so as to allow for effective metabolic
cooperation, two or more spatially non-contiguous entities may nonetheless
qualify as a joint individual that is maintained over time. That said, however, the
further apart the constituent parts are in space, the weaker their cooperative
interactions are and as a result, the more marginal the metabolic individuality of
the joint system is (Godfrey-Smith, 2013b).
Crucially, in order for highly cooperating parts that are also metabolic
individuals themselves to become a joint metabolic individual, some degree
of their metabolic independence must be partially or temporarily ‘surren-
dered’ for that of the higher-level metabolic individual or as Godfrey-Smith
writes:
If a whole system has a highly organismal form of integration, if it is a whole

with respect to its metabolic activity, then its parts must, necessarily, be less
organismal [less of a metabolic individual]. Those parts must be highly inter-
dependent, less able to function as metabolic whole themselves. (2013a: 26;
my insertion)
And conversely, if the parts of a system exhibit a high degree of independ-

ence with respect to maintaining themselves metabolically, this reduces the
degree to which the joint system they comprise qualifies as a metabolic
individual. Whilst inside the squid, V. fischeri are highly dependent on the
squid for food; the nocturnal hunting success of the bobtail on the other hand
is dependent on the bacteria, during the period of the diel cycle in which the
bacteria populate the squid’s cavity. When the squid expels most of the
bacteria in the morning, it and any given expelled bacterium (or bacteria) are
metabolically independent again and thus no longer jointly qualify as
a metabolic individual.
There is one last important aspect of Godfrey-Smith’s analysis of biological
individuals that is worth mentioning: although there are cases in which
biological individuals are either a metabolic individual or a Darwinian indi-
vidual, there can be biological individuals that are both (see also Ereshefsky
and Pedroso, 2015). For example, whereas a gene is a Darwinian individual
but not a metabolic individual, a bobtail squid–V. fischeri symbiotic
association is a metabolic individual but not a Darwinian individual (i.e., there

is no parent–offspring lineage common to both symbionts because they
reproduce independently). On the other hand, a honeybee colony may not
only qualify as a Darwinian individual to some degree but, given that the
colony is a metabolically integrated system with a division of metabolic
labour among its interacting bee parts, it may also be viewed as exhibiting
a non-zero degree of metabolic individuality (cf. Seeley, 1989).
Having reviewed Darwinian and Metabolic individuals, let us now turn to the
task of evaluating whether the plasmodial dyad in the cases of fragmenting and
fusion (or non-fusion) qualifies as either a Darwinian individual and/or a metabolic
individual.
4.2 Evaluating the Plasmodial Dyad

Recall the possible behavioural patterns described earlier: a single plasmodium
fragments into two separate cells after reaching two spatially separate food
sources. Subsequent to consuming the food sources, these cells are likely to
fuse, forming one larger plasmodial cell. The puzzle to be addressed is whether
the plasmodial dyad is a biological individual above and beyond the two
plasmodial cells which the dyad consists of.
Let us start with considering whether the dyad counts as a Darwinian indi-
vidual (or has some degree of Darwinian individuality). A plasmodium is
a unicellular multinucleate organism. During cell growth, its nuclei continu-
ously reproduce via mitosis without cell division. However, unlike bodily cell
division, which can occur independently of the particular extracellular milieu
(e.g., in a Petri dish), nuclear division cannot occur outside of the cell environ-
ment. This suggests that Physarum nuclei are scaffolded reproducers according
to Godfrey-Smith’s framework. Since it only contains scaffolded reproducers,
a single plasmodial cell qualifies as a simple reproducer. Given that only
collective reproducers can themselves be made up of other entities that can
make more of themselves by way of their own reproductive ‘machinery’ (i.e.,
collective, and/or simple reproducers), a collective reproducer is the most
reasonable option of the three reproducer categories to base an evaluation of
the plasmodial dyad upon. Rephrasing the question above more precisely in
terms of Darwinian individuals: is the plasmodial dyad a collective reproducer
(at least to some degree) that is composed of simple reproducers?
One reason to answer this question negatively is that the two plasmodial cells,
despite being genetic clones, are independent lineage formers. Thus, there is no
feature that unites them as a collective reproducer. To see this, consider the
features that Godfrey-Smith introduces to adjudicate collectively reproducing
Darwinian individuals. The two plasmodial cells score null for germ line; there is
no division of reproductive labour that the two spatially separate cells exhibit;
each cell is able to reproduce and do so independently of the other. The dyad has
a similar score for both reproductive bottleneck (a narrowing that marks the
beginning of a new generation) and integration (i.e., spatial boundedness).31
These scores across all three features suggest that the dyad is not itself
a collective lineage-forming system. In other words, the dyad is a mere group
and not the kind of thing that reproduces as a unit and/or takes part in the process
of evolution by natural selection. Does the plasmodial dyad stand a better chance
of exhibiting some degree of metabolic individuality?
This question boils down to one of whether or not the two plasmodial cells
engage in some degree of metabolic cooperation. At first blush, it seems that
neither member of the plasmodial dyad reciprocally interacts with the other,
metabolically integrating in the service of the dyad’s continued existence. One
might expect this to be the case since the two plasmodia making up the dyad,
unlike, say, symbiotic associations or different honeybee castes, are homoge-
neous members that share the same features (i.e., clones). Accordingly, it might
be thought that neither plasmodial fragment cell can provide the other with
something that it cannot already provide itself and thus interaction between
homogeneous parts does not lend itself to a cooperative metabolic division of
labour (cf. Godfrey-Smith, 2013a). This, however, I would like to argue is too
fast. In the next section, I will show that limiting the evaluation to the features of
the dyad in isolation from what occurs prior (fragmentation) and subsequent to it
(fusion or non-fusion) obscures the big picture – a picture which is necessary for
recognising potential instances of at least one unusual form of metabolic indi-
viduality. Seeing the big picture means recognising patterns of plasmodial behav-
iour as they occur over time, taking more generally what has become known as
a processual view of biological individuality (see Meincke and Dupré, 2020).
4.2.1 Fragmentation, Fusion, and Non-fusion Patterns

The two different plasmodial behavioural patterns that will be used in what follows
to evaluate metabolic individuality in plasmodia I will call fragmentation-fusion
(FF) and fragmentation-non-fusion (FN) patterns. I have included simplified
diagrammatic schemas of FF and FN in Figure 6. The first pattern, FF, represents
one initial plasmodial cell at t1 that spreads out and covers two spatially distant
food sources at t2. After a period of consuming food, the t2 cell fragments into two
31
The dyad is not a bottleneck since it is a doubling in cell number relative to the fragmenting
plasmodium.
Figure 6 Plasmodial fragmentation-fusion (FF) schema: arrows represent different

events. The first set of arrows represent a spreading event that results in a one
distributed plasmodial cell that covers both food sources at t2. The second set of
arrows represents fragmentation event that results in two spatially separate
plasmodial cells at each food source location at t3. The third set of arrows represents
a fusion event in which the dyad at t3 merge to form a single plasmodial cell at t4.
The colour version of this figure is available at www.cambridge.org/Sims
Figure 7 Plasmodial fragmentation-non-fusion (FN) Schema: all events up to t3

are identical to FF. The third set of arrows represents non-fusion event. The
colour version of this figure is available at www.cambridge.org/Sims
fully separate cells at t3 that continue to consume the two food sources independ-
ently. After the food has been consumed, the t3 cells fuse at t4 (see Figure 6).
The second pattern, FN, is identical to FF except that the two plasmodia, after
consuming the separate food sources at t3, do not fuse at t4 but continue to live as
independent cells (see Figure 7). One result of what I am calling non-fusion is
that the two cells become resource competitors. This can even potentially lead
to one of the two cells consuming the other (see Clark and Haskins, 2012).
I will now show how evaluating the metabolic individuality of plasmodial dyad
in the larger contexts of FF and FN reveals an interesting possibility that is
consistent with viewing the dyad at t3 as a spatially non-contiguous metabolic
individual. Let’s put some flesh on the bones of this way of looking at FF and FN.
4.2.2 Evaluation of the Dyad in the Context

of FF and FN Patterns
Recall that fragmentation between t2 and t3 occurs after a plasmodial cell has reached
and partially consumed, spatially separated food sources. Thus, fragmentation is a
behaviour that occurs in response to separate food sources. What kinds of conditions
would affect whether fragmentation occurs after the cell reaches the two food
sources? One condition, but not the only one I suspect, has to do with the distance
between the food sources relative to the size of the plasmodial cell. If the distance
separating the food sources is significantly shorter than the size of the cell, then the
cell could cover both sources without needing to extend itself in any manner. On
the other hand, if the distance between the food sources is significantly greater
than the overall size of the cell, then to cover and consume both sources simultan-
eously, the cell must plastically modify its shape to reach both sources. It is only in
this latter ‘stretched out’ case that fragmentation would seem to benefit the cell in
exploiting both resources. In other words, ‘network shape is the solution to the
organism’s survival problems’ (Nakagaki et al., 2004: 2305).
If the cell at t1 can reach both food sources by altering its morphology and
connecting the two sources, what is the benefit of fragmenting? One possible
answer, and not the only one, is that the shuttling of protoplasm between the
spatially distributed regions of the plasmodial cell when it has covered both
food sources is metabolically expensive and may slow down the process of
consuming each of the sources of food (cf. Nakagaki et al., 2004); that is, in
certain foraging landscapes two smaller cells may be more efficient at consum-
ing each food source simultaneously than a larger stretched-out cell is.
Therefore, if fragmentation offers a benefit that is contingent upon both the
size of the cell and the length of the distance between the food sources, then
fragmentation in response to food may be viewed as a behavioural strategy for
efficient food consumption.
Fragmentation in plasmodia, when extending across two distant food
sources, is driven by changes in internal protoplasmic shuttling (Section 2)
that reallocate cytoplasm, nutrients, and other cellular components towards
separate growth regions (Nakagaki et al., 2001). With reduced protoplasmic
flow between the two regions that are in contact with the food, the vein-like
tubule that connects them decays, resulting in the fragmenting of the cell. Does
this mean that fragmentation is something that happens to the cell, rather than
something that the cell actively does? There is a compelling reason to think that
fragmentation is, in fact, under the cell’s behavioural control. Protoplasmic
shutting is how a plasmodium normally locomotes, in addition to how it forages
and explores its environment. It is an underlying behavioural mechanism. As
such, the fact that changes in protoplasmic shuttling underwrite fragmentation
fails to be a reason to view fragmenting as something other than controlled
behaviour – any more than it is a reason to deny that locomotion, foraging, or
exploring are controlled behaviours. Fragmenting in this case is something that
a plasmodial cell does and not something that merely happens to it.
Thus far, the description of the behavioural pattern, from t1 to t3, is common
to both FF and FN. The difference between the two patterns is paramount to
evaluating plasmodial metabolic individuality. In the case of FF, the two cells of
the dyad fuse at t4. This is something that would be expected to occur given that
the cells originated from the same larger cell (i.e., they are genetic clones) and
that no mutations accumulated in the short period of time since fragmentation,
rendering them too genetically different to fuse (cf. Clark and Haskins, 2012).
What is relevant here is that fusion can occur at t4 because the cells of the dyad
are clones (closely genetically related if not identical). When the two cells fuse,
something interesting happens. The cell boundary separating the two adjacent
cells begins to degrade and the protoplasm shuttling tubules from each cell
begins to connect with the other cell’s tubules. As this occurs, the ‘fruit’ of each
cell’s metabolic labour is reciprocally shared as protoplasm flows through the
connecting tubules. During the final step of complete fusion, the two cells can
no longer be distinguished from the larger plasmodial cell that they become; the
cells lose their metabolic (and Darwinian) individuality for that of the larger
plasmodial cell they become at t4.
Recall that metabolic individuals persist over time despite turnover of mater-
ials and, more generally, change. Varying degrees of metabolic integration of
interacting parts (i.e., cooperation) is the functional ‘glue’ of the persisting
individual. The plasmodial cell at t1 and at t2, respectively, have high degrees of
metabolic cooperation amongst their intracellular parts. Similarly, the fused
plasmodial cell at t4 is also a highly metabolically integrated unit. It is not
immediately obvious, on the other hand, how each cell of the dyad at t3 may
metabolically cooperate with the other given the fact that each cell’s metabolic
machinery is highly autonomous. On closer inspection and when placed in the
context of FF, however, there is a precursory process which enables subsequent
metabolic integration and is mediated by the shared environmental substrate
that the two cells occupy. Although this precursory process is not itself direct
metabolic integration (it does not affect either cells’ metabolic activity), it
counts as a form of indirect metabolic integration when placed in the context
of FF. How might this be the case?
Plasmodia exude various biochemicals such as calcium into the substrate
upon which they locomote and rest (Vogel et al., 2015; Briard et al., 2020). In
a lab setting, this substrate is typically ‘agar’ (i.e., a non-living gelatinous
substance that is derived from seaweed) that covers the bottom of a Petri dish.
It has been shown that biochemicals that diffuse into a substrate can be used as
cues by those plasmodia which detect them to guide their navigational behav-
iour. More precisely, if the plasmodium which leaves the biochemical cue is
stressed (e.g., starved), then the cue will elicit an aversion response on the part
of the plasmodium that detects it. On the other hand, if the plasmodium that
exudes the biochemical is well-nourished, then the cue acts as an attractant.
Being an attractant means that a plasmodium that detects it will be likely
to approach the source of the diffusing biochemical gradient (Vogel et al.,
2015; Briard et al., 2020). Sometimes this source will be the plasmodium that
left the cue.
With this in mind, and returning to FF, if each separate plasmodial cell that
consumes the spatially separate food sources exudes a cue that acts as an
attractant (or a repellent) for the other, relaying the condition of the plasmodium
that left the cue, then it seems that in addition to genetic similarity, the
physiological condition of the two plasmodia can affect whether or not they
fuse. Given the use of environment-mediated chemical cues that lead to
fusion of the two cells in FF, I would like to suggest that there is a sense in
which the two separate cells have a degree of indirect metabolic integration.32
Importantly, such indirect integration occurs only when both plasmodial cells
leave and use cues that are attractive and, as a result, pave the way for subse-
quent fusion to occur.33 In this sense, calcium may play a similar role in
indirectly integrating spatially separate plasmodia as autoinducers produced
by V. fischeri during quorum-sensing play in indirectly integrating bacteria and
bobtail squid prior to bioluminescence of the squid–Vibrio individual.
Putting all of the pieces together: the occurrence of fragmentation followed
by fusion, FF, I would like to argue, licenses viewing fusion as the reforming of
the plasmodial cell that fragmented. The plasmodial dyad, if this is correct,
despite being homogeneous parts, represent a spatial division of metabolic
labour on the part of the fragmenting plasmodium. When the plasmodium at
t2 fragments, it persists as a higher-level metabolic individual comprised of the
two cells (lower-level metabolic individuals), metabolically benefiting as a unit
from the behaviour of each of its non-contiguous parts only after fusion. There
is a degree of indirect metabolic integration between the two separate plasmo-
dial cells at t3. However, and in contrast to the orthodox view of metabolic
individuality, what matters most in the case of FF is that the fruit of each cell’s
metabolic labour is shared during subsequent fusion. If this is correct, then FF
represents an interesting case in which an initially high degree of direct meta-
bolic integration of the plasmodial cell at t1 and t2 is temporarily interrupted at
t3 and then subsequently re-established at t4. This temporary interruption also
means a substantial temporary decrease in the degree of metabolic independ-
ence (and hence metabolic individuality) of the persisting higher-level dyadic
32
See Seeley (1989) on honeybee colony integration via cues and shared environment.
33
It follows that such indirect metabolic integration would not occur if the two cells were separated
by a large distance or if they were unable to detect and respond to each other’s cues.
individual during the period in which it is only indirectly integrated. In contrast,

each cell of the dyad that is produced as a result of fragmentation has a high
degree of metabolic independence (and metabolic individuality) until they fuse.
This temporary interruption of the initially high degree of direct metabolic
integration and its re-establishment can be viewed as an exhibition of plastic,
metabolism-driven behaviour on the part of the fragmenting individual –
a metabolic individual that is maintained over FF despite being spatially non-
contiguous. The phenotypic plasticity exhibited by Physarum at the various
stages across its life cycle, as we saw in Section 2, and the highly plastic
behaviour of plasmodia in particular (as documented by Nakagaki et al.,
2001; Dussutour et al., 2010; Latty and Beekman, 2011; Vogel and Dussutour,
2016), provide some additional support for this interpretation, at least in theory.
Lastly, what about FN – something that cannot be ruled out from occurring
a priori? When fusion fails to occur after the cells of the dyad have consumed
the separate food sources, we may infer that a full loss of indirect metabolic
integration has occurred during t3. In failing to fuse, the fruit of each of the cell’s
metabolic labour cannot be shared but is instead used by each cell independently
as it becomes a resource competitor with the other. Thus, whether the dyad
qualifies as a metabolic individual is contingent upon the occurrence of FF,
something which is underwritten by environment-mediated indirect metabolic
integration.
This kind evaluation may not sit right with some. One might argue that in the
case of FF it is more intuitive to view the fragmenting individual as ceasing to
exist after fragmentation, with a new metabolic individual being created when
and only when the two resulting cells fuse at a later time. While this alternative
evaluation may seem intuitive, its being so is less indicative of its correctness
and more indicative of the fact that the forms which metabolic individuals take
can often strain our intuitions. The ease with which our intuitions can change
and pull in opposite directions under slightly different conditions illustrate that
they are not a reliable metric for determining all cases of biological individual-
ity. For example, our intuitive sense of whether the same pre-fragmentation
individual persists during the separation and after fusion may depend on the
duration of separation. If FF occurs over hours, it might intuitively seem that the
fragmenting individual does not persist. However, if FF would occur over
a period of seconds, we might intuit the opposite. This inconsistency raises
the questions: how long must the two cells be apart before the pre-fragmenting
and post-fusion plasmodia are considered distinct individuals? How quickly
must they fuse to qualify as a single continuous individual? The lack of clear,
non-arbitrary answers suggests that intuition alone is not a reliable guide when it
comes to such a case of metabolic individuality (or biological individuality
more generally). Although the evaluation that I have proposed may be less
intuitive than the alternative, this by itself is no reason to prefer the latter.34
One might still object that, regardless of differences in intuitions, this evalu-
ation unnecessarily multiplies metabolic individuals in a way that the simpler
alternative does not, thus dulling Occam’s razor. The proposed evaluation posits
three coexisting metabolic individuals after fragmentation (the two separate
cells of the dyad and the joint individual that they constitute), whereas the
alternative posits only two (each cell of the dyad). Although simplicity is
generally viewed as a value in scientific explanation and evaluation, it does
not necessarily mean that simpler evaluations (or explanations) are always
preferable. In the context of biological individuality, the notion of simplicity
must be approached with caution. Take for example the symbiotic association
between the bobtail squid and V. fischeri: if one considers this – as many
philosophers of biology do – a transient metabolic individual, one implicitly
acknowledges a nested individual, the existence of which is above and beyond
that of the squid and its numerous bacterial symbionts. All such analyses of
symbiotic associations, however, are rendered dead in the water if simpler
evaluations are viewed as inherently superior. Moreover, the very question of
whether a symbiotic association is a metabolic individual (or a Darwinian
individual) turns out to be ill-posed under the assumption the simpler evalu-
ations trump all others. Given that we continue to pose interesting questions
about metabolic individuality regarding systems like symbiotic associations –
questions that play a role in legitimate scientific theorising – I do not see why the
plausibility of the proposed evaluation should be dismissed because it is less
simple than the alternative.35
4.3 Moving Beyond the Orthodoxy

Taking the proposed evaluation onboard requires expanding the orthodox view
of metabolic individuals and rethinking how metabolic independence (auton-
omy) is exhibited at different adjacent levels of a biological hierarchy. In the
orthodox account of metabolic individuality that I have described, it is par for
the course to evaluate whether some group of metabolic individuals is a higher-
level, collective metabolic individual by taking into account the metabolic
34
Perhaps the idea that a metabolic individual is spatially non-contiguous is one source of
discomfort with the proposed solution. It should be remembered, however, that this idea is not
by any means a unique feature of the particular solution that I have argued for; it is generally
acknowledged that metabolic individuals can be spatially non-contiguous. Ant colonies are one
such example that will be explored in Section 5.
35
Many thanks to an anonymous reviewer for encouraging me to discuss this alternative way of
evaluating FF.
integration of its constituent parts. What is not taken into account, however, is
whether the constituent parts have a shared beginning and whether or not it is
typical for those parts to have a shared end. More precisely, the evaluation of
metabolic individuality that is typical of the orthodox view does not take into
account whether the entities being evaluated are the products of fragmentation
and whether those entities are likely to fuse together subsequent to exercising
their independent metabolic machinery.
Perhaps one reason for this is that the problem cases for metabolic individuality
(or more generally for physiological individuality) that philosophers and biolo-
gists have tended to focus on evaluating have often taken the form of symbiotic
associations of various calibres. Symbionts, being heterospecific, are not them-
selves the products of fragmentation events of a monospecific organism. Another
reason may be as simple as rarity of occurrence. Although asexual reproduction
via fragmentation is common in a number of taxa ranging from some plants,
animals, and fungi, what is much less common is the combination of organism-
initiated fragmentation and subsequent fusion of those fragments.36 In the case
of FN, absence of fusion suggests that FN events end up being an instance of
asexual reproduction. When the combination of fragmenting and subsequent
fusion occurs, fragmentation may be seen as a form of plastic, metabolism-
driven behaviour. Physarum plasmodia (and myxomycetes more generally)
may be unique in exhibiting both fragmentation and fusion. Assuming that the
FF pattern would occur given that fragmentation and fusion occur separately, the
orthodox notion of metabolic individual may be stretched to its limit in this
particular case.
4.4 A Counterfactual Metabolic Analysis

If I am correct, contextualising the dyad suggests that metabolic integration can
sometimes take a different form from that which is often the focus of the
orthodox view of metabolic individuality; it can be indirect. Evaluating this
different form of integration is ultimately tied up with knowing what happens
next in the sequence of events, knowing whether or not fusion occurs after
fragmentation. In this sense, whether FF or FN occurs determines whether the
plasmodial dyad is or is not a joint metabolic individual. Although metabolic
integration between the cells is indirect during the period in which they are
separate, what matters in this case is that their independent metabolic activities
contribute to the larger biological individual that they jointly maintain.
36
Sponges can fuse sometimes when conditions are suitable after fragmentation due to damage.
However, since it is damage that causes fragmentation rather than something that the sponge
itself does in response to separate food sources, such a pattern differs significantly from FF.
It is only after the two cells have fused – if they do – that we can look back at
their behaviour as representing a division of metabolic labour that the higher-
level individual comprised of the two cells benefits from as a unit. Thus,
whether or not the dyad is a metabolic individual is contingent upon what
would occur after fragmentation. I would like to suggest that when adjudicating
the metabolic individuality of the dyad at t3 without knowing what happens
next, the best we can settle for is a counterfactual analysis. This may take
something like the following form:
Counterfactual analysis of metabolic individuality: if fusion of two plas-

modial cells originating from the same fragmenting plasmodium would occur
sometime after food resource exploitation, then the two plasmodial cells
qualify as a single metabolic individual.
Importantly, that fusion is not guaranteed to occur subsequent to fragmentation

(although it is likely) calls important attention to the idea that evaluation of
metabolic individuality must sometimes occur on a case-by-case basis. While
the best method that we may be able to deploy when considering the metabolic
individuality of any fragmented plasmodium cell prior to its fusing (or not
fusing) is a counterfactual analysis, the actual evaluation of metabolic individu-
ality must be made a posteriori and does not generalise to all cases. Thus, the
puzzle of plasmodial fragmentation and fusion has a backwards-facing solution.
Turning to the next and final section of this Element, we shall look at another
fascinating instance of highly plastic plasmodial behaviour – one that has
gained the interest of biologists, philosophers, and cognitive scientists: the use
of extracellular slime trails for navigating complex environments.
5 Externalised Spatial Memory?

Over the last two decades, Physarum has become a model system for investi-
gating the possibility of various cognitive capacities in non-neuronal organisms
(Dussutour, 2021; Reid, 2023). One motivation for carrying out such studies is
made explicit in the increasingly popular research programme of ‘basal cogni-
tion’ (Lyon et al., 2021). The idea behind basal cognition is to investigate
potential exercises of capacities such as learning, memory, anticipation, and
decision making in non-neuronal organisms with the aim of identifying shared
mechanisms that underwrite both complex cognitive capacities found in ani-
mals and those simpler capacities found in non-neuronal organisms.37 For
37
In what follows, I will assume the following working definition of cognition: ‘Cognition
comprises the sensory and other information-processing mechanisms an organism has for
becoming familiar with, valuing, and interacting productively with features of its environment
[exploring, exploiting, evading] in order to meet existential needs, the most basic of which are
example, it is posited that some mechanisms underwriting neuronal information

processing may be highly evolutionarily conserved, dating back to similar
mechanisms in early free-living cells (Levin, 2019). Moreover, there is the
live possibility that functionally similar cognitive capacities that are exhibited
in a wide range of organisms could be the result of convergent evolution
(Dussutour, 2021). Thus, one way of approaching the study of cognition and
cognition-like capacities (but by no means the only way) is to examine instances
in which simple organisms like Physarum flexibly and adaptively direct their
behaviour in response to sensed changes in environmental conditions.
Numerous studies looking in particular at the behaviour of Physarum plas-
modia have shown that they exhibit various capacities to process information
that have been hitherto only observed in animals. Despite lacking either
a nervous system and/or a fixed shape, individual plasmodial cells have been
observed to find the shortest path between food sources in different legs of
a maze (Nakagaki et al., 2000), to become habituated to aversive stimuli
(a simple form of learning) (Dussutour, 2021), to make complex foraging
decisions (Latty and Beekman, 2011), and to engage in a form of anticipatory
behaviour (Saigusa et al., 2008). These results suggest that a plasmodium does
not mechanically and invariably respond to its environment by way of stimulus-
response pathways; rather, it evaluates multiple environmental conditions that it
encounters and uses those evaluations to flexibly guide its behaviour in ways
that are consistent with its continued viability.
One capacity that has garnered the attention of both biologists and philo-
sophers, something that was briefly mentioned in Section 2, is Physarum’s
ability to use its secreted extracellular slime to direct its navigation in a way
that allows it to avoid revisiting previously foraged areas (Reid et al., 2012).
Some researchers have proposed that extracellular slime functions as an exter-
nalised spatial memory for plasmodia when navigating through complex envir-
onments (Reid et al., 2012; Smith-Ferguson et al., 2017; Sims and Kiverstein,
2022). This interpretation challenges the conventional view of memory in
cognitive science and psychology as being an internally stored structure (e.g.,
an ‘engram’, trace, etc.) – a structure traditionally associated in neuronal
organisms with strengthened synaptic connections and, more recently (and
more contentiously), associated with macromolecules such as non-coding
RNA in both neuronal and non-neuronal organisms (see Gershman, 2023).
Setting this internalist assumption aside, in this section, I would like to focus
upon two primary questions about the relationship between memory, cognition,
survival/persistence, growth/ thriving, and reproduction’ (Lyon et al., 2021: 4). Awareness, on
this characterisation, is not a requirement of cognition.
and learning raised by the cognitive interpretation of Physarum’s interaction

with its extracellular slime. More precisely, such an interpretation prompts us to
consider what makes memory a part of a cognitive process (i.e., subject to
cognitive explanation), and whether memory always results from some form of
learning. Using Reid et al.’s experiment as a jumping off point, it is my aim in
this section to show how addressing each of these questions can be informative
about addressing the other.
This section will be organised as follows: firstly, I will describe the details of
Reid et al.’s (2012) experiment. Then I will consider the two primary questions
regarding memory’s relation to learning and cognition that Physarum’s inter-
action with its extracellular slime brings to the fore. After suggesting one way of
differentiating memory that is subject to cognitive explanation from that which
is not using degrees of metabolic individuality (Section 4), four different
categories of biological memory will be articulated and used to construct
a fourfold memory analysis. Lastly, this analysis will be used to situate Reid
et al.’s experimental results.
5.1 Reid et al.’s 2012 Physarum Experiment

A notable characteristic of plasmodia is their tendency to leave behind a visible
residue of extracellular slime as it moves through its environment. Taking this
into account, Reid et al. posed the question of whether a Physarum plasmodium,
upon encountering extracellular slime, employs it as a guide to steer away from
previously explored areas that may have been depleted of nutrients. To investi-
gate this question, these researchers conducted experiments under two different
conditions to assess how the use of extracellular slime influenced the speed of
a plasmodium in successfully reaching a food source (glucose). In the first
condition (referred to as the ‘blank’ condition), they lined the Petri dish with
untreated agar, placing a drop of glucose solution (the ‘goal’) on top. As it
defused within the agar, this glucose created an attraction gradient that the
plasmodium could follow to navigate to the food source. A U-shaped acetate
trap was then positioned on the agar’s surface between the food source and the
starting point of the plasmodium. Since plasmodia do not move as efficiently
over dry surfaces, this dry acetate trap acted as an obstacle to reaching the
glucose source. In the second condition (referred to as the ‘coated’ condition),
the set-up was the same except that the agar was coated with a layer of
extracellular slime. In both conditions, Reid et al. measured the time it took
for Physarum to successfully reach the goal.
The researchers hypothesised that if extracellular slime was indeed used by
Physarum to avoid revisiting previously explored areas, then the time taken to
reach the food source would be significantly longer in the coated condition
compared to the blank condition. This is because the slime-treated agar would
obscure the plasmodium’s own extracellular slime tracks. Remarkably, Reid
et al. discovered that the average time that a plasmodium spent migrating across
areas of agar it had previously explored was nearly ten times longer in the
coated condition than in the blank condition. According to Reid et al., these
findings ‘offer a unique demonstration of a spatial memory system in a non-
neuronal organism, supporting the theory that an externalised spatial memory
may be the functional precursor to the internal memory of higher organisms’
(2012: 1). Is extracellular slime really memory, and if so, is it the kind of
memory that is significant to the study of cognition?
Here is one working definition of biological memory offered by biologists
Frantisek Baluška and Michael Levin:
Memory is defined as experience-dependent modification of internal structure,

in a stimulus specific manner that alters the way the system will respond to
a stimulus in the future as a function of its past. (Baluška and Levin, 2016: 902)
The fact that extracellular slime is a structure located outside of a plasmodium

places its status as memory at odds with this characterisation of biological
memory – a characterisation which seems to honour the internalist assumption
common to traditional cognitive science and psychology that all cognitive
processes occur inside the boundaries of an organism. There have been
a number of arguments foisted against this assumption which I take to be
compelling and thus I will not rehearse them here (see Clark and Chalmers,
1998; Sims and Kiverstein, 2022). It should be noted that this characterisation of
biological memory is both phyletically neutral, and it rules out just any tempor-
ally contingent response (e.g., a broken bone) from counting as memory due to
its emphasis on stimulus specificity (cf. Colaço, 2022). Moreover, this charac-
terisation does not distinguish memory as a cognitive capacity from memory
that is not. In fact, the process of experience-dependent structural modification
referred to ‘may or may not involve a degree of intelligence’ (Baluška and
Levin, 2016: 902).38 One question that arises then is what distinguishes memory
qua cognitive capacity from memory that is not?
Getting some purchase on this question is crucial for warranting a cognitive
interpretation of extracellular slime and its use. Since Physarum’s use of
extracellular slime could represent a form of non-cognitive memory, Reid
et al.’s claim that it is a kind of externalised spatial memory may be much less
of a thorn in the side of traditional accounts of memory in cognitive science and
38
Within the context of their article, Baluška and Levin (2016) do not distinguish cognition from
intelligence. I will follow them here.
psychology, both of which focus upon investigating memory qua cognitive

capacity. If this is the case, the task of distinguishing ‘cognitive memory’
from ‘non-cognitive memory’ becomes one of utmost importance.
Another telling feature of Baluška and Levin’s characterisation of biological
memory is the notion that structural modification is experience-dependent. Note
that it is left open as to whether experience arises by way of learning or by some
other means in which an environmental factor affects an organism’s future
behavioural tendencies. Moreover, if learning is taken to be a necessary condi-
tion for memory, it rules out viewing extracellular slime as memory (either
cognitive or non-cognitive) because plasmodial secretion of extracellular slime
is not a structural modification that results from learning.39 Thus, an initial
answer to one of the primary questions above is suggested by Baluška and
Levin’s definition: not all memory is the result of learning.
In the next section, I will propose one way of distinguishing cognitive
memory from non-cognitive memory in biological systems that is based on
the notion of metabolic individuality discussed in Section 4.40 I will then turn to
few examples that buttress the claim that memory needn’t be the result of
learning. This will put us in a better place to understand where Physarum’s
use of extracellular slime stands with respect to its status as a form of memory.
5.2 Why Cognitive Memory Arises at the Level

of the Metabolic Individual
As suggested by Baluška and Levin, not all memory qualifies as a cognitive
process and hence there are some forms of memory which fall out of the scope
of cognitive explanations. I would now like to suggest that one thing that
distinguishes memory as a cognitive capacity from other forms of biological
memory is that the former is something that arises at the level of an integrated
metabolic individual and only marginally at the level of the subsystems making
up that metabolic individual.
Recall, from Section 4, that a metabolic individual is an entity that is made up of
metabolically integrated parts that work together in the service of that individual’s
persistence despite the continuous turnover of matter. Metabolic individuality
comes in degrees as measured by the presence of a system’s own metabolic
machinery, metabolic integration of parts, and autonomy of metabolic functioning.
39
Whereas extracellular slime is considered to be a medium for information storage, the causal
interaction between a plasmodium and extracellular slime has been argued to represent a form of
recall or what has been called ‘memory making’ (Sims and Kiverstein, 2022).
40
For my purposes in this section, the notion of metabolic individuality that I shall use will be
indifferent to what was called the ‘orthodox’ view and the expanded view that was argued in
Section 4 is required to make sense of fragmentation and fusion patterns.
Metabolic individuals can be, but needn’t be reproducers (i.e., Darwinian individ-
uals), thus allowing for some heterospecific symbiotic associations that do not
reproduce as a unit to nonetheless qualify as delineable units of function. Relatedly,
metabolic individuals can be nested; a highly metabolically integrated individual
can be made up of other metabolic individuals; however, those at lower organisa-
tional level(s) give up some of their metabolic independence (i.e., autonomy) for
the continued functioning of the individual at the higher level. Taking all of these
core features into account, how might the notion of metabolic individuality hint at
where cognitive explanations of memory might get the most purchase? If metabolic
individuals are first and foremost persisters (Godfrey-Smith, 2013a), and such self-
maintenance is the fundamental background against which all cognitive capacities
might be thought to arise (Lyon et al., 2021; Sims, 2023), then it would seem that
the kind of memory (learning and decision making for that matter) that warrants
possible cognitive explanation qua cognitive process is that which arises at the level
of a metabolic individual (cf. Keijzer, 2021).
This suggestion requires some refining however: although this rules out
entities that are clearly not metabolic individuals such as genes, viruses, and
genetic regulatory networks, because metabolic individuality is a matter of
degree, an immediate challenge to this approach is that it requires drawing
a non-arbitrary line between how much metabolic individuality is required to
warrant memory being subject to cognitive explanation and how much is too
little. Whilst I am sceptical that such a non-arbitrary line can be drawn, there is
another way to decide upon the matter. It involves considering levels of
biological organisation and their relative degrees of metabolic individuality.
Even if some entity qualifies as a marginal metabolic individual, the fact that it
is part of a larger system which has an even higher degree of metabolic
individuality would suggest that the behaviour of the organisational level with
the highest degree of relative metabolic individuality would be subject to
explanation in terms of cognitive memory. To be clear, being subject to cogni-
tive explanation means that the observed memory can be tested or investigated
using criteria from specific theories of cognition (e.g., criteria for spatial
memory, procedural memory, etc.). Satisfying those criteria, however, is an
additional step, and one that can fail. On the other hand, if an entity fails to be
a metabolic individual or fails to score as having the highest degree of relative
metabolic individuality, investigating its observed memory using cognitive
theories would constitute a category error.
Next, we will consider what this suggests about where the use of cognitive
explanation of memory is warranted across different levels of biological organ-
isation, beginning with bodily cells then and working up to groups of metabolic
individuals. Two questions will be addressed at each level: (1) how is memory
exhibited and (2) does the entity/entities occupying that specific level qualify as
a metabolic individual?
5.3 Using Metabolic Individuality to Identify the Appropriate

Level for Cognitive Explanations
5.3.1 Somatic Cells and Cellular Memory
In contrast to germ cells, somatic cells undergo differentiation during develop-
ment, giving rise to various cell types that collectively form the tissues, organs,
fibres, and bone structures of multicellular organisms. Each somatic cell of
a specific type can produce daughter cells of the same type through the process
of development and cell division (mitosis). While it is true that the genetic
information encoded in the DNA of each cell contributes to the organism’s
overall structure, somatic cell differentiation relies on more than just the genetic
code. This is where the concept of cellular memory earns its salt.
‘Cellular memory’ refers to the mechanisms that ensure the stability and
preservation of specific characteristics and functions in differentiated cells as
they go through mitosis (D’Urso and Brickner, 2014). These mechanisms often
involve epigenetic modifications to gene function that are not the result of
changes in DNA sequence (e.g., DNA methylation and histone modification)
(Jablonka and Lamb, 2020). Cellular memory helps explain how a particular
somatic cell type and its lineage maintain their unique identity during develop-
ment and across cell division, allowing for the diversity and specialisation of
cells in multicellular organisms. Is the cellular memory of somatic cells an
example of cognitive memory? This depends, or so I would like to argue, on
whether somatic cells are metabolic individuals (or have a high degree of
metabolic individuality).
Somatic cells possess their own metabolic machinery and can perform basic
metabolic processes independently to a certain degree, as demonstrated by their
ability to be cultured in vitro. However, successful cultivation of somatic cells
in a laboratory setting necessitates the creation of a controlled environment that
replicates bodily conditions. In the natural bodily environment, the cooperation
and metabolic interaction among different somatic cells and cell types are
essential for each cell’s physiological function. While somatic cells have their
own metabolic machinery, their continued operation and viability rely heavily
on constant metabolic integration with other cells and organs. For instance,
a heart cell indirectly depends on cells in the stomach and small intestine to
obtain metabolites from digested food, facilitated by the bloodstream. Thus,
somatic cells, despite having their own metabolic machinery, are highly inte-
grated into and metabolically dependent upon a larger metabolic system and
cannot be considered bona fide metabolic individuals. This suggests that their
cellular memory is not subject to cognitive explanation.
This conclusion is consistent with acknowledging that cellular memory can
be fruitfully modelled ‘as if’ it was a cognitive process (cf. Pezzulo and Levin,
2016). However, due to the evolutionary path that somatic cells have followed,
favouring the suppression of their metabolic independence in favour of the
autonomy of the larger metabolic entity they constitute (such as the organism),
treating them as cognitive agents, if I am correct, bottoms out as a useful fiction
(e.g., helping to identify and highlight similar underlying mechanisms in use).
5.3.2 Immune Systems and Immunological Memory
The immune system is a complex network composed of cells, organs, and

signalling molecules found in all multicellular organisms. Its primary role is to
serve as a defence mechanism against various pathogens, such as harmful
bacteria, viruses, and parasites. When these invaders are detected, the immune
system deploys immune cells to eliminate them. To understand the concept of
immunological memory, it is essential to consider the idea of ‘affinity matur-
ation’. This refers to the process by which certain immune cells, due to the
specific conformation of their membrane receptors, have a stronger attraction to
pathogens (Paul, 2003). In simpler terms, these immune cells have receptors that
match the 3D shape of the antigens on the pathogen’s surface. When these cells
‘recognise’ a pathogen, they release biochemical signals that are received by
other immune cells. These signals convey information about the identity of the
encountered pathogen, enabling the immune system to mount a targeted response.
Crucially, immune cells with a higher affinity for pathogens undergo more
controlled mutation during cell division than those with lower affinity. As a result,
over several generations of cell division, the immune cell line with higher
pathogen affinity becomes even more specialised and effective. These immune
cells have longer lifespans and form part of a repository known as ‘immuno-
logical memory’ (Farber et al., 2016). When an organism encounters the same
pathogen in the future, the immune cells within the immunological memory can
respond rapidly and effectively to eliminate the specific pathogens or any similar
pathogens with antigens that share a similar protein conformation.
Is the immune system a metabolic individual and, more to the point, does it have
a degree of metabolic individuality that is greater than that of the organism in
which it is situated? I think the answer is a resounding no. Like other somatic cells,
immune cells do have their own metabolic machinery and a certain degree of
metabolic autonomy. That said, the long-term functioning of metabolic processes
and persistence of the network of immune-specific cells and molecules that make
up the immune system is dependent upon their being functionally integrated within
an organism; the immune cells with high pathogen affinity that are maintained in
the immune memory repertoire, for example, require energy and nutrients to
function, which are supplied by various non-immune system cells and tissues.
Relative to the organism that harbours immune cells, the continued functioning of
their metabolic machinery is tied up with the encompassing organismal system
within which the immune system has evolved to function as a part of. Therefore,
like the cellular memory of somatic cells within a multicellular organism,
immunological memory of the immune system, I would like to argue is not subject
to cognitive explanation for the same reason.
5.3.3 Organisms and Organismal Memory
The vast majority of memory research in cognitive science and comparative

psychology has been focused on metazoans such as humans, primates, rats,
pigeons, corvids, sea slugs, and nematodes – paradigmatic organisms. Such
research has investigated organismal memory using behavioural change to
operationalise memory (Shettleworth, 2010), in addition to studying encoding,
storage, and recall by way of identifying possible neuronal mechanisms
(Gershman, 2023; Colaço and Najenson, 2023). Assuming that all organisms
are metabolic individuals that exhibit a higher degree of metabolic individuality
than their parts, and that explanations in terms of cognitive memory are
warranted at the level of biological organisation where there is the highest
relative degree of metabolic individuality, that organisms represent the paradig-
matic biological level at which cognitive memory research has been investi-
gated should come as no surprise. I shall assume the claim that organismal
memory is indeed subject to explanation in terms of cognition and is therefore
uncontroversial and spills no further ink on the matter here. There is, however,
a question as to whether collections of organisms can exhibit an even higher
relative degree of metabolic individuality than organisms.
5.3.4 Ant Colonies and Collective Memory

Eusocial insect societies, exemplified by certain ant, bee, and termite species, can
be characterised as socially integrated colonies that involve multiple generations
living together, cooperating in offspring care, and exhibiting a division of repro-
ductive labour where non-reproductive ‘workers’ assist reproductive ‘queens’
(Wilson and Hölldobler, 2005). The idea that such societies can be viewed as
biological individuals can be traced at least as far back as W. M. Wheeler’s (1911)
now-classic article ‘The ant colony as an organism’. This idea has been developed
since then with some biologists and philosophers viewing various eusocial
colonies as ‘superorganisms’ (Willson and Sober, 1989). These are groups of

individual organisms that exhibit behaviours only arising at the level of the
collective (e.g., complex foraging patterns, colony defence, reproduction, etc.)
(also see Gordon, 2010). This brings us to the questions of whether a eusocial ant
colony can be seen as exhibiting memory at the level of the colony and, if so,
whether such memory should receive treatment as a cognitive process? Let’s take
each of these questions in turn.
Research by biologist Deborah Gordon seems to support an affirmative answer
to the first question. Using Harvester ants (Pogonomyrmex barbatus), Gordon
(1989) conducted a series of disturbance experiments in which she strategically
interfered with the various tasks of different workers. When toothpick obstacles
were placed, it led workers to move them; when trails were blocked, foraging
efforts on the part of foragers increased; when a disturbance was created it lead to
attempts by patrollers to suppress those disturbances. While each experiment
directly affected only one worker group, the behaviour of other groups of workers
altered because the activity of workers allocated to one task is dependent upon the
rate of brief encounters with workers doing other tasks (Gordon, 1989). Strikingly,
after a few days of repeating the experiment, it was observed that the colonies
maintained the altered behaviour (i.e., switching tasks and nest positions) in the
absence of the disturbances and only gradually did the undisturbed task allocation
patterns resume. The changing behaviour of the colony suggests that although
individual ants may not retain any memory of the disturbance, a colony-level
memory of the disturbance was formed (Gordon, 2018).
Is such colony-level memory the kind of memory that can be subject to
cognitive explanation? Answering this question, if what I have been arguing is
correct, involves evaluating whether the colony can be viewed as a metabolic
individual and if it has a higher degree of metabolic individuality relative to the
individual ants making up the colony or the system which the colony is a part of.
Firstly, I think that an ant colony can be viewed as a metabolic individual for at
least three reasons using the concept of metabolic individuality reviewed in
Section 4: (1) a colony is made up of heterogeneous parts (i.e., ants with different –
yet flexible – task allocations) that function together so as to maintain the colony
despite turnover of individual parts (ants); (2) there is a high degree of cooper-
ation and metabolic integration between those parts – something that is evidenced
by Gordon’s disturbance experiment; and (3) metabolic integration of parts – at
least in some colonies – is underwritten by various attractant or repellent bio-
chemical marks (e.g., pheromones signals) (Sumpter and Beekman, 2002),
colony-level reciprocal food sharing in the form of ‘trophallaxis’ (i.e., the oral-
oral and oral-anal exchange of nourishing fluids) (LeBoeuf, 2017), and rate of
entering and exiting the nest (Gordon, 2010).
Assuming that there is no colony-containing biological system that scores

higher than the colony in terms of metabolic individuality, the question to focus
upon is whether a colony scores higher in terms of being a metabolic individual
than an individual ant? I would like to argue that ants and colonies come close to
having a similar score, close enough to regard memory in either of them as
subject to cognitive explanation. This depends on whether an ant is functioning
as a part of a colony or is isolated from the colony. When functioning in the
colony, an ant ‘surrenders’ some of its metabolic independence for that of the
colony. The nature of colony life is highly cooperative, such that the distribution
of tasks (defence, nutritive, etc.) has viability benefits for most of the individual
ants in the colony. Such dependence on the colony suggests that it has a higher
score relative to an individual ant. Individual ants, however, have not evolved in
such a way that their metabolic independence has become fully supressed for
colony-level metabolic autonomy or cannot be regained to a degree if an ant
finds itself isolated from its colony. Unlike somatic cells or an immune system,
ants in a colony have not evolved within a spatial boundary. This spatial degree
of freedom may allow individual ants to retain their independence as metabolic
individuals while simultaneously allowing them to be part of a highly integrated
metabolic superorganism, the task-allocation flexibility of which is dependent
upon the ant parts maintaining their metabolic individuality and spatial degree
of freedom.
Taking these points into account, I would like to suggest that both the colony-
level memory and individual ant memory are subject to cognitive explanation.
Importantly, this does not necessarily mean that they will conform to specific
criteria demanded by various cognitive memory theories. Rather, it means that it
is not a category error to apply such criteria to them. The determination of this
matter is likely to hinge on careful examination of the broader task, such as
navigation, in which memory is employed. This task may often involve learn-
ing, but sometimes not, as we shall now see.
5.4 Memory as a Result of Learning versus Memory

as a Result of Inheritance
Learning may be understood broadly as a form of information processing that
results in experience-dependent changes of behaviour as adapted to local
environmental conditions (Dussutour, 2021). It includes, but is not limited to,
processes like conditioning, habituation, sensitisation, and trial-and-error learn-
ing. Setting aside, momentarily, the question of whether the particular kinds of
memory mentioned are subject to cognitive explanation, let us consider whether
learning plays a part in each of them. Starting with cellular memory that
constrains somatic cell differentiation through development and over mitosis:

while early differentiating cells may learn in response to encountering epigen-
etic factors via their relative position to other cells, the memory possessed by
cell progeny is not the result of learning; rather, it is the result of the progeny’s
inherited epigenetic marks that persist over mitosis. Immunological memory
may be seen as a result of learning. Immune system cells detect pathogens and,
due to affinity maturation and controlled mutation of cells with higher pathogen
affinity, information regarding pathogens is stored and used to direct the
system’s future immune responses.
On some occasions organismal memory can be the result of learning. For
example, conditioning, where repeatedly encountering stimulus–stimulus pairs
separated by a time interval across a training period, is representative of the kind
of cognitive psychology textbook understanding of how memory is formed. On
other occasions organismal memory can be the result of inheritance without
learning. This is clear in cases of say memory transfer where memory has been
experimentally induced via ‘artificial inheritance’. For instance, Physarum plas-
modia that have been repeatedly exposed to a non-lethal amount of an aversive
stimulus learn to ignore it and, thus, become habituated to the specific stimulus.41
It was shown that when a habituated plasmodium fuses with a plasmodium that
has not been habituated, the larger post-fusion cell responds in a habituated
manner (Vogel and Dussutour, 2016). Similarly, memory transfer has been
shown to occur with ‘sensitisation’ or a decrease in response threshold based
on prior experience. RNA taken from a trained Aplysia californica (a kind of giant
sea slug) that learned to respond to shock with a longer siphon withdraw reflex
when injected into an untrained Aplysia resulted in the naïve Aplysia responding
to the shock in the same sensitised manner (Bédécarrats et al., 2018). In each of
these cases memory directs behaviour without learning having occurred in the
transferee.
Lastly, what about ant colony memory? In the case previously described,
memory of the colony seems to result from learning at the level of the colony.
Such learning and memory are underwritten by ‘interaction dynamics’ (i.e., the
rate of interaction and rate of response) between various ants performing different
tasks in the colony (Gordon, 2010). Such interaction dynamics can include not
only interaction with other ants but also interaction with environment-mediated
signals (pheromone trails) left by ants that iteratively affect the nature of such
dynamics (Sumpter and Beekman, 2002). All of this is compatible with the fact
that individual ants can learn and direct their navigational behaviour according to
41
More precisely, habituation occurs when there is a decrease in response to a specific cue to
repeated encounters with that stimulus.
visual cues in the environment (Aron et al., 1993). Such learning may contribute
to colony-level memory that can remain stable for many years, ‘outliving’ the
individual ants that contributed to the formation and stabilisation of the colony
memory (see Rosengren and Fortelius, 1987).
5.5 A Fourfold Analysis of Biological Memory

Using the results of the analyses in Sections 5.3 and 5.4, there are four possible
categories of memory which are thrown into relief: memory subject to cognitive
explanation, memory that is not subject to cognitive explanation, memory that
results from learning, and memory that does not result from learning. These
opposing memory category pairs can be situated along two dimensions, illus-
trating how they interact within a fourfold analysis of biological memory
(Table 3). There are some cases that are more clearly subject to cognitive
explanation than others. Making a decision regarding the latter cases will likely
depend upon how memory is used in the wider context of a particular task and
hence satisfying the criteria for the specific form of memory (e.g., spatial
memory, etc.) being investigated.
Returning to the cognitive interpretation of Reid et al.’s experiment: if what
I have argued here is correct, given that a Physarum plasmodium scores higher
with respective to metabolic individuality than its parts (e.g., nuclei) or higher
than any other biological system which it is a part of, it follows that
a plasmodium’s use of extracellular slime as it navigates across complex
environments falls into the category of memory that is subject to cognitive
explanation and that is not the result of learning. Such memory represents a
paradigm example of external niche construction (ENC) (Section 2).
6 Conclusion
Philosophy of biology brims with a panoply of interesting and difficult puzzles,
challenging much of our quotidian understanding of the biological world. This
Element has served as a starting point and a full-bodied exercise in illustrating
how attention to the outlier model organism – the acellular slime mould,
P. polycephalum – can go a long way in terms of bringing some of those puzzles
to the fore; a long way in providing concrete cases with which to consider just
how wondrous and wondrously unintuitive the biological world can be. Given
that biological theory is not an island that is somehow isolated from our pre-
theoretical assumptions, the work that Physarum can do does not stop at
challenging folk biological assumptions. This Element represents a mere
scratching of the perennial surface when it comes to how Physarum can
contribute to the philosophy of biology. If it has piqued the interest of the
Table 3 A fourfold analysis of memory and some examples
Memory subject to cognitive explanation Memory not subject to cognitive explanation
Memory that Cases of trial-and -error learning, habituation and Associative conditioning at levels below the metabolic individual
results from conditioning at the level of the organism (e.g., conditioning in gene regulatory networks (Biswas et al., 2021))
learning (e.g., habituation in P. polycephalum (Vogel and Dussutour, 2016); Conditioning at levels below the highest scoring metabolic individual
habituation in Stentor coeruleus (Rajan et al., 2023); trial-and-error (e.g., associative learning in purkinje cells (Jirenhed et al., 2017))
learning in Stentor roeseli (Jennings, 1902; Dexter et al., 2019); Immunological memory (e.g., primed antibody response to pathogens at
conditioning in Paramecium aurelia (Gelber, 1962; Armus et al., level of immune system (Cohen, 1992))
2006); conditioning in Amoeba proteus (de la Fuente et al., 2019); Some cases of learning at the level of the colony or ‘superorganism’
conditioning in Caenorhabditis elegans (Morrison et al.,1999); and (?)
conditioning in dogs (Pavlov, [1897] 1902))
Some cases of learning at the level of the colony or ‘superorganism’
(e.g., learned task reallocation in response to perturbation
(Gordon et al., 1989))
Memory that does Transferred memory that results in matching behavioural profile in Epigenetically stabilised somatic cell differentiation and development
not result from transferee to that of the trained individual that learned (e.g., epigenetic regulation in pluripotent stem cells (Watanabe et al.,
learning (e.g., Physarum fusion habituation transfer (Vogel and Dussutour, 2013))
2016); sensitisation transfer in Aplysia (Bédécarrats et al., 2018)) Transgenerational cellular memory (e.g., proliferation and maintenance of
Production and use of environmentally mediated cues and signals for heterogeneity in bacterial cell characteristics over multiple generations
spatial navigation (e.g., Physarum’s production and use of due to epigenetically inherited marks (Vashistha et al., 2021))
extracellular slime to navigate complex environments
(Reid et al., 2012, 2013))
philosopher to look further into the fascinating life cycle and behaviour of slime
mould, if it has inspired the biologist to consider the deep philosophical
challenges made salient by Physarum, or if it has provided some common
ground for future research that both the philosopher and the biologist can
tread upon in tandem, then ‘Slime Mould and Philosophy’ has done its job.
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Acknowledgements
I would like to thank the following people for the many discussions that shaped this
Element and for providing comments on either all or parts of the manuscript: Jan
Baedke, Nick Brancazio, David Colaço, Si Qiao Ding, John Dupré, Audrey
Dussutour, Carrie Figdor, Debora Gordon, Jeremy Gunawardena, Eva Jablonka,
Fred Keijzer, Michael Levin, Pamela Lyon, Kevin Mitchell, Kathryn Nave, Emma
Otterski, Guido I. Prieto, Sofiia Rappe, Chris Reid, Tobias Schlict, Caroline
Stankozi, Tobias Starzak, Stephen Stevenson, and Alejandro Fárbregas Tejeda.
A very special thanks to two anonymous reviewers for their helpful comments
and to Grant Ramsey and Michael Ruse for their support and encouragement to
write this Element. Lastly, I am grateful to Benjamin Little for his unwavering love
and being a constant source of inspiration. This research was made possible through
generous support from the VolkswagenStiftung.
Philosophy of Biology
Grant Ramsey
KU Leuven
Grant Ramsey is a BOFZAP research professor at the Institute of Philosophy,
KU Leuven, Belgium. His work centers on philosophical problems at the foundation of
evolutionary biology. He has been awarded the Popper Prize twice for his work in this area.
He also publishes in the philosophy of animal behavior, human nature and the moral
emotions. He runs the Ramsey Lab (theramseylab.org), a highly collaborative research
group focused on issues in the philosophy of the life sciences.
Michael Ruse
Florida State University
Michael Ruse is the Lucyle T. Werkmeister Professor of Philosophy and the Director
of the Program in the History and Philosophy of Science at Florida State University. He is
Professor Emeritus at the University of Guelph, in Ontario, Canada. He is a former
Guggenheim fellow and Gifford lecturer. He is the author or editor of over sixty books,
most recently Darwinism as Religion: What Literature Tells Us about Evolution; On Purpose;
The Problem of War: Darwinism, Christianity, and their Battle to Understand Human
Conflict; and A Meaning to Life.
About the Series

This Cambridge Elements series provides concise and structured introductions to
all of the central topics in the philosophy of biology. Contributors to the series are
cutting-edge researchers who offer balanced, comprehensive coverage of multiple
perspectives, while also developing new ideas and arguments from a unique viewpoint.
Philosophy of Biology
Elements in the Series

Evolution, Morality and the Fabric of Society
R. Paul Thompson
Structure and Function
Rose Novick
Hylomorphism
William M. R. Simpson
Biological Individuality
Alison K. McConwell
Human Nature
Grant Ramsey
Ecological Complexity
Alkistis Elliott-Graves
Units of Selection
Javier Suárez and Elisabeth A. Lloyd
Evolution and Development: Conceptual Issues
Alan C. Love
Inclusive Fitness and Kin Selection
Hannah Rubin
Animal Models of Human Disease
Sara Green
Cultural Selection
Tim Lewens
Matthew Sims
A full series listing is available at: www.cambridge.org/EPBY

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Sims

Physarum polycephalum, also known more colloquially as ‘the

Slime Mould and Philosophy

Cover image: Ascidiae from Kunstformen der Natur (1904)

SLIME MOULD AND

Cambridge University Press is part of Cambridge University Press & Assessment,

Elements in the Philosophy of Biology

Abstract: Physarum polycephalum, also known more colloquially as

Keywords: slime mould, philosophy of biology, niche construction, biological

© Matthew Sims 2024

2 Niche Construction and Complex Life Cycles 4

3 On the Biotic Status of Spores 25

4 Biological Individuals: A Puzzle Concerning Plasmodial

5 Externalised Spatial Memory? 60

Physarum’s use of its extracellular slime trails as a form of memory – and if so

1.1 What Is P. polycephalum?

Table 1 Taxonomic classiﬁcation

Figure 1 P. polycephalum plasmodium: a giant, yellow, unicellular

2 Niche Construction and Complex Life Cycles

face. Since whether some phenotypes evolve in a population is at least partly

2.1 Niche Construction: An Overview

for the evolution of those large rodents we know as beavers? By constructing

acknowledging what is called ‘ecological inheritance’. This refers to ‘the

2.2 Three Kinds of Niche Construction

2.3 Complex Life Cycles

Alternation of generations is apparent in Physarum’s life cycle as ameboﬂagel-

2.4 Stages of Physarum’s Complex Life Cycle

Figure 2 Stages of P. polycephalum’s complex life cycle: (1) spore;

Myxamoebae locomote on surfaces by pulling and pushing themselves with

2.5 Three Kinds of Niche Construction Exempliﬁed

construction are related: CNC may allow an organism to temporarily compen-

The microcysts stage is also an optional manner that an ameboﬂagellate can

instance of CNC, so may the structural modiﬁcation of a plasmodium in response

as a kind of niche construction? Although not as straightforward as the previous

2.6 The Value of Looking at Complex Life Cycles

Life cycle Relations between niche

Life cycle Relations between niche

patterns between those relations becomes possible in such a context. To stress,

3 On the Biotic Status of Spores

3.1 Is Metabolism a Requirement for Life?

a living system is an object with a deﬁnite boundary, continually exchanging

A living system, according to this deﬁnition, is one that is delimited by

Yet, another example of how metabolic exchange is viewed as an essential

By metabolism we understand the active or passive entrance of material and

Similar to Sagan’s standard metabolic deﬁnition, Gánti’s necessary (but not

An autopoietic machine is a machine organised (deﬁned as a unity) as

components which: (i) through their interactions and transformations con-

presence of these commonalities which allow using an investigation into

3.2 Putting Metabolism on Temporary Hold

A system suitable for the occurrence of the processes in question may be

evergreens, octopuses, humans, and bacteria, all undoubtable examples of life

3.3 Being Alive versus Living

That [remaining stable in a non-living state] tells us something about the

Lane’s characterisation of the difference between life and living in terms of

3.4 Dead, Structura Vivens, or Living: A Taxonomy

Figure 3 Dead, alive, or living (DAL) taxonomy – conceptual space: life

3.4.1 Generalising the DSVL Taxonomy

course of spore development (the zoomed-in perspective). This is because of the

3.5 Spore Ageing

Figure 5 A mirroring of spore ageing and senescence in vegetative cells. The