Driscoll2015 PDF

Ecology Letters, (2016) 19: 8197
doi: 10.1111/ele.12533
REVIEW AND
SYNTHESIS
William W. Driscoll,1,2,3*
Jeremiah D. Hackett3 and
gis Ferri
Re
ere2,3*
1
Department of Ecology, Evolution
and Behavior, University of

Minnesota St. Paul, 5106 MN, USA
2
rieure Institut
Ecole Normale Supe
de Biologie de lENS (IBENS), CNRS
UMR 8197, 46 rue dUlm, Paris,
F-75005, USA
3
Department of Ecology and
Evolutionary Biology University of

Arizona Tucson, 85716 AZ, USA
*Correspondence: E-mail:
wwdriscoll@gmail.com (or)
ferriere@biologie.ens.fr
Eco-evolutionary feedbacks between private and public goods:

evidence from toxic algal blooms
Abstract
The importance of eco-evolutionary feedbacks in natural systems is currently unclear. Here, we
advance a general hypothesis for a particular class of eco-evolutionary feedbacks with potentially
large, long-lasting impacts in complex ecosystems. These eco-evolutionary feedbacks involve traits
that mediate important interactions with abiotic and biotic features of the environment and a selfdriven reversal of selection as the ecological impact of the trait varies between private (small scale)
and public (large scale). Toxic algal blooms may involve such eco-evolutionary feedbacks due to
the emergence of public goods. We review evidence that toxin production by microalgae may yield
privatised benefits for individual cells or colonies under pre- and early-bloom conditions; however, the large-scale, ecosystem-level effects of toxicity associated with bloom states yield benefits
that are necessarily public. Theory predicts that the replacement of private with public goods
may reverse selection for toxicity in the absence of higher level selection. Indeed, blooms often
harbor significant genetic and functional diversity: bloom populations may undergo genetic differentiation over a scale of days, and even genetically similar lineages may vary widely in toxic
potential. Intriguingly, these observations find parallels in terrestrial communities, suggesting that
toxic blooms may serve as useful models for eco-evolutionary dynamics in nature. Eco-evolutionary feedbacks involving the emergence of a public good may shed new light on the potential for
interactions between ecology and evolution to influence the structure and function of entire
ecosystems.
Keywords
Eco-evolutionary dynamics, eco-evolutionary feedback, multiscale dynamics, public good,
sociomicrobiology, toxic algae bloom.
Ecology Letters (2016) 19: 8197
INTRODUCTION
Interactions between ecological and evolutionary processes

can lead to population- and community-level phenomena that
cannot be understood on the basis of each process operating
in parallel (Fussmann et al. 2007; Schoener 2011). One particularly intriguing possibility is that ecological and evolutionary
change may feedback to reciprocally influence one another
(Reznick 2013). Such eco-evolutionary feedbacks can be
described by using three ingredients: (1) heritable traits that
affect some ecological properties of the system, (2) ecological
modifications that are persistent and strong enough to alter
selection on the traits, and (3) an actual adaptive response of
these traits to the change in selection (Ferriere et al. 2004;
Kokko & L
opez-Sepulcre 2007). We call eco-evolutionary
dynamics the dynamics of ecological and evolutionary
variables when such a closed feedback loop operates between
ecological and evolutionary processes (Smallegange &
Coulson 2013).
Over the last 10 years, the development of several model
systems has facilitated direct tests of theoretical models of
eco-evolutionary feedbacks and dynamics (Ellner 2013). However, the significance of these processes for natural ecosystems
remains unclear due to the relative scarcity of field studies.
(Strauss 2014). In particular, the spatial and temporal scales

of eco-evolutionary feedbacks, and the impact of these effects
on the structure and function of natural ecosystems, remain
largely unknown (De Meester & Pantel 2014). Strauss (2014)
echoed Fussmann et al. (2007) and Schoener (2011) when she
stated, our biggest challenge remains to understand how
often and when ecoevolutionary dynamics could be expected to have large, longlasting impacts in complex field ecosystems (Strauss 2014).
This essay explores toxic algal blooms as potential natural
demonstrations of eco-evolutionary feedbacks centred around
the emergence of widely distributed public goods. We begin
by describing a general hypothesis for a particular class of
eco-evolutionary feedbacks with potentially large, long-lasting
impacts in complex field ecosystems. Next, we review evidence from the harmful algae literature for eco-evolutionary
feedbacks involving private and public aspects of toxin production. We then provide several (brief) illustrations of the
key elements of this feedback from a broad range of ecological systems, including plant and animal communities, as well
as laboratory microbes. We consider the implications of the
lack of obvious terrestrial analogues for toxic algal blooms,
both for the existence of these processes, as well as our ability
to detect and measure them over practical timescales. Finally,
2015 John Wiley & Sons Ltd/CNRS
82 W. W. Driscoll et al.
we highlight major challenges and opportunities within and

beyond the field of toxic algal bloom research.
THE CONCEPT OF EMERGENT PUBLIC GOODS IN
ECO-EVOLUTIONARY FEEDBACKS
Here, we introduce a simple conceptual framework to explain

the role of emergent public goods in eco-evolutionary feedbacks. We focus on the very simple case of a costly trait
within a polymorphic population that positively influences
direct interactions between individuals and some aspect of
their environment. An eco-evolutionary feedback may arise
when the following conditions are met:
(1) The trait is favoured by natural selection in sparse populations due to individual-level advantages (private good);
(2) The distribution of benefits extend beyond the level of individuals due to novel ecological effects of the trait, which
may be triggered by local increases in population density or
other changes in ecological context (positive feedback);
(3) Selection reverts to favour conspecifics that do not bear
the focal trait (public good).
(4) The decline of individuals expressing the trait contributes
towards restoring the system to the initial state (tragedy
of the commons).
In this scenario, a trait that primarily impacts direct interactions at the level of individuals shifts to yield public benefits
at broader levels (e.g. subpopulations or entire communities).
However, these larger scale (and potentially long-lasting)
benefits may obviate the original, individual-level functions,
ultimately undermining the privatizable aspects of the trait.
Because an individualistic trait gives way to a true public
good not by evolutionary change (i.e. the evolution of cooperation), but through ecological change, we call this an emergent
public good, in contrast with an evolved public good. We present a graphical representation of this hypothesis in Box 1,
and discuss relationships with established concepts from
evolutionary game theory in Box 2.
EMERGENT PUBLIC GOODS AND ECOEVOLUTIONARY FEEDBACKS IN TOXIC ALGAL
BLOOMS
Although humans have known of toxic algal blooms (TABs)

for (at least) hundreds of years, the frequency and severity of
blooms is increasing as a result of anthropogenic nutrient
loading, pollution and climate change (Paerl & Huisman
2009). For our purposes, we operationally define a toxic
bloom as a dramatic increase in the density of one or a few
species of microalgae, at least one of which produces toxins
that negatively impact other members of the native plankton
community. (We are not concerned with non-toxic algae
blooms that are harmful as a result of physical properties of
1
We are unaware of toxic unicellular green algae, although the multicellular
genera Ulva and Ulvaria do produce toxic blooms (Nelson et al., 2003).
2
We follow Flynn et al. (2013) in reserving the term mixotroph to refer to
organisms that engulf particulate organic material (phagocytosis), excluding
lineages that take up dissolved organic material through osmotrophy, as this
latter group appears to include virtually all autotrophic microalgae.
Review and Synthesis
the cells, or due to byproduct effects of extreme densities (e.g.

anoxia).)
Toxic blooms may occur in virtually any aquatic environment with adequate nutrients. The diversity of environments
impacted by TABs is matched by the phylogenetic and ecological diversity of the causative organisms themselves: the
prokaryotic cyanobacteria and members of two of the three1
major photosynthetic eukaryotic phyla (alveolata and
stramenopiles) are known to cause toxic blooms. Microalgal
toxins are similarly diverse in structure (including cyclic peptides (Jungblut & Neilan 2006), fatty acids, and alkaloids (Van
Dolah 2000)), mode of action (they may attack lipid bilayers,
block specific ion channels or mimic neurotransmitters (Van
Dolah 2000)), and deployment (toxins may be retained
intracellularly, injected into targets, or actively secreted).
Several long-held assumptions about blooms and the organisms that cause them are currently being challenged on the
basis of molecular data, microscopic observations, and theoretical modelling. Blooms had commonly been viewed as the
result of adaptive strategies of entire, genetically homogenous populations (Thornton 2002); however, recent advances
in molecular biology have revealed the surprising genetic and
taxonomic heterogeneity of toxic blooms. Concurrently, a new
appreciation for the sophistication with which individual cells
wield toxins for defensive and offensive purposes has focused
new attention on the cell (rather than population) as an
important ecological agent. Finally, the (still common) distinction between phytoplankton and zooplankton is increasingly questioned as examples of mixotrophic (combining
autotrophy with heterotrophic acquisition of nutrients) species
accumulate (Flynn et al. 2013). Indeed, mixotrophs2 are particularly well represented among TAB-forming eukaryotes
(Stoecker 1999; Graneli 2006; Burkholder et al. 2008).
Below, we briefly review key aspects of TAB ecology and
evolution through the lens of four key assumptions of the
emergent public goods hypothesis: (1) Toxin production is
advantageous for individual cells (or colonies) under certain
conditions (private good), (2) Increasing toxicity and cell density result in large-scale ecological changes that further benefit
toxic populations (positive feedback), (3) Benefits extend to
the surprising diversity of genotypes and phenotypes within
the blooming population, including non-toxic, resistant
lineages (public good), and (4) Non-toxic, resistant cells that
benefit from the emergent public good may undermine the
public good (tragedy of the commons).
The benefits of toxin production can be privatized
We highlight two basic classes of cell-level functions3 of toxicity: defensive (grazing deterrent) and offensive (assistance in
predation). Both offensive and defensive cell-level functions
have been demonstrated under laboratory conditions for
several important species of toxic microalgae (Table 1).
3
Some important microalgal toxins may serve unrelated functions, and negatively influence other organisms only as a byproduct; for example, domoic
acid produced by diatoms appears to function as an iron chelator (Rue & Bruland 2001).
Private/public goods in eco-evolutionary dynamics 83
Toxicity as chemical defence: deterring choosey predators
Animal and microbial predators4 exert strong top-down

controls on the standing biomass of primary producers in
most aquatic environments (Cyr & Face 1993; Polis 1999;
Shurin et al. 2006). It is therefore not surprising that, like
their terrestrial counterparts, planktonic algae have evolved
numerous physical, behavioural and chemical defences
against predation. Chemical defences vary considerably in
regulation, structure and mode of action, and include the
potent neurotoxins implicated in paralytic and diarrhoetic
shellfish poisoning (Van Dolah 2000). As in terrestrial
plants, many microalgae dynamically regulate toxin production in response to specific or general grazing signals,
presumably minimising metabolic/physiological costs (Van

Donk et al. 2011).
Many important predators show a surprising ability to
preferentially avoid, reject or expel toxic prey at the level of
individual cells or colonies: zebra mussels (Vanderploeg et al.
2001), Daphnia (Haney & Lampert 2013), copepods (Teegarden 1999), rotifers (Kirk & Gilbert 1992) and unicellular
predators (Strom et al. 2003; Graham & Strom 2010) are all
capable of rejecting toxic prey in mixtures with nontoxic
prey (Table 1). These selective predators may play important
roles in maintaining toxicity within populations by selectively
targeting low-toxicity strains (Teegarden 1999). Furthermore,
selective grazing may play a key role in bloom initiation by
favouring toxic lineages over non-toxic competitors
Box 1 A graphical model of emergent public goods through eco-evolutionary feedbacks.
Ecological state
(e.g. population size)
Eco-evolutionary feedbacks consist of three ingredients: (1) heritable traits that affect some ecological properties of the system,
(2) ecological modifications that persist long enough and strongly enough to alter selection on the traits, and (3) an actual
adaptive response of these traits to the change in selection.
Multiple related frameworks are available to model these eco-evolutionary dynamics (Dieckmann & Law 1996; Metz et al.
1996; Abrams 2000; Dercole et al. 2002; Hairston et al. 2005; Champagnat et al. 2006; Cortez & Ellner 2010). Eco-evolutionary
modelling highlights the importance of the traits-to-ecology map (the ecology map, in short), which translates ingredient (i);
and the traits 9 ecology-to-fitness map (the fitness map, in short), which captures ingredient (ii). Figure 1 schematically illustrates how these maps together determine the expected eco-evolutionary equilibrium [or equilibria, and/or more complicated
attractor(s)] in a constant environment.
Mean trait value

Figure 1 Ecological and evolutionary ingredients in eco-evolutionary modelling. In this simple depiction, the evolutionary dynamics develop along a
single-trait axis (horizontal) and the ecological dynamics develop along a single state variable (such as population density) axis (vertical). The plain,
thick curve (blue) is the trait-to-ecology map, which represents the equilibrium ecological state as a function of the trait. Vertical (blue) arrows indicate
that the equilibrium is stable at all values of the trait. The dashed, thin curve (red) is (the zero contour of) the trait 9 ecology-to-fitness map (or fitness
map); it is the locus of trait and population size at which the selection gradient is zero. Horizontal (red) arrows indicate that the selection gradient is
positive below the fitness map, and negative above. The filled circle indicates the eco-evolutionary equilibrium arising in this graphical example.
Figure 2 depicts the interaction between ecological and evolutionary change in the context of emergent public goods. In
Fig 2ad, the ecology map is S-shaped to indicate the existence of alternative ecological states, such as low vs. high equilibrium
population density, over a range of trait values. The S-shape is meant to capture the existence of tipping points (threshold
effects) of high density and/or high toxicity: for a given toxicity (within the appropriate range), the large-scale ecological effects
of sufficiently high density can drive the population from one stable state (e.g. low density) to another stable state (e.g. high
density). This scenario could be realised by positive feedbacks between density and net growth rate, which are generally relevant
to the onset of toxic blooms.
4
We use the word predator, rather than the more common word, grazer,
to refer to organisms that consume microalgae, because the microalga is necessarily killed when it is eaten. We note that organisms that consume
microalgae have historically been called grazers, perhaps because their prey
is photosynthetic, or perhaps because the distinction between entire organ-
isms and parts of organisms is less clear in planktonic autotrophic communities (which include colonies, filaments and aggregates) than their terrestrial
counterparts. Given our focus on commonalities and contrasts between aquatic and terrestrial communities, we opt for semantic consistency.
Box 1 Continued
Ecological state
(a)
(e)
Response to environmental fluctuation

(b)
(c)
(d)
(f)
Mean trait value

Figure 2 Alternative eco-evolutionary scenarios yielding emergent public goods. Open circles indicate the location of eco-evolutionary equilibria prior to
environmental perturbation, and dotted curves indicate instability (ecological instability along the ecology map, or divergent selection around the fitness
map). In (ad), the ecology map is S shaped, with alternate ecological equilibria over a range of trait values. In (a), prior to environmental
perturbation, the eco-evolutionary equilibrium is on the lower (i.e. low density) branch. In (bd), some environmental perturbation shifts the ecology
map (b), the fitness map (c), or both (d). As a result, there is positive (negative) selection on the trait at low (high) density, triggering a wide ecoevolutionary oscillation (grey arrows). In (ef), there are no alternative ecological equilibria in the ecology map. Instead, instability in both ecology and
fitness maps (f) can cause stable eco-evolutionary limit cycles when ecological and evolutionary change occur over similar timescales.
In Fig. 2a, the fitness map intercepts the ecology map on its lower stable branch, thus predicting a stable eco-evolutionary
equilibrium of low density and intermediate toxicity. Figure 2bd illustrates the destabilisation, and potential re-stabilisation of
the original eco-evolutionary equilibrium as caused by the emergence of a public good. This may happen through shifts in the
ecology map (Fig. 2b), the fitness map (Fig. 2c), or both (Fig. 2d), thus relocating the fitness map in between the two stable
branches of the ecology map. Following destabilisation, higher toxicity evolves (private good of Step 1 in the emergent public
goods sequence) whilst the population density increases modestly, thus remaining in the low density state. At some critical
threshold of toxicity, the low-density equilibrium becomes unstable and the system shifts to its alternate ecological stable state
(high density; positive feedback of Step 2). At high density, there is now selection against toxicity (public good of Step 3),
which leads eventually to the collapse of the population on to its original (low density) ecological state, with reduced toxicity
(tragedy of the commons of Step 4). A similar type of eco-evolutionary hysteretic cycle was first described by Dercole et al.
(2002) in a different biological context (evolution of body size in a competitive system).
Figure 2 emphasises that each of these shifts may be caused by some environmental perturbation. In Figure 2b, the environmental perturbation moves the ecology map upward; this might be the result of some nutrient input, which would cause an
increase in density independently of the trait value, or circulation patterns that cause the formation of dense cell aggregations.
In Figure 2c, the environmental perturbation moves the fitness map upward, as a consequence of selection becoming more
favourable to toxicity at low density. This might be caused by increased densities of prey, such as soft-bodied algae. This change
causes higher competition for inorganic nutrients, but simultaneously results in greater availability of organic nutrients derived
from intraguild predation. Both changes favour increased reliance on toxin-mediated predation. Because shifts in the ecology
and/or fitness maps may not be permanent, the system is predicted to return to its original eco-evolutionary equilibrium as the
effects of the environmental perturbation dissipate. This might occur at various points along the cycle, thus potentially generating a rich array of bloom dynamics, varying notably in their duration and toxicity at the onset of the termination phase.
Finally, Figure 2e and f underscore that the existence of alternate stable ecological states is not strictly required. In Figure 2f,
both the ecology and fitness maps are destabilised, causing the replacement of the original eco-evolutionary equilibrium with a
stable limit cycle. Steps 14, however, still apply to the four different phases of the cycle (increase in toxicity, increase in
density, decrease in toxicity and decrease in density).
(Teegarden et al. 2001; Vanderploeg et al. 2001). Indeed,

introduced (Schoenberg & Carlson 1984) and native (Wang
et al. 2010) selective predators can promote the growth of
toxic cyanobacteria in natural communities, underscoring the

potential for the indirect effects of selective predation to
facilitate TABs.
Box 1 Continued
Ecological state
(a)
(e)
Response to environmental fluctuation

(b)
(c)
(d)
(f)
Mean trait value

Figure 2 Alternative eco-evolutionary scenarios yielding emergent public goods. Open circles indicate the location of eco-evolutionary equilibria prior to
environmental perturbation, and dotted curves indicate instability (ecological instability along the ecology map, or divergent selection around the fitness
map). In (ad), the ecology map is S shaped, with alternate ecological equilibria over a range of trait values. In (a), prior to environmental
perturbation, the eco-evolutionary equilibrium is on the lower (i.e. low density) branch. In (bd), some environmental perturbation shifts the ecology
map (b), the fitness map (c), or both (d). As a result, there is positive (negative) selection on the trait at low (high) density, triggering a wide ecoevolutionary oscillation (grey arrows). In (ef), there are no alternative ecological equilibria in the ecology map. Instead, instability in both ecology and
fitness maps (f) can cause stable eco-evolutionary limit cycles when ecological and evolutionary change occur over similar timescales.
In Fig. 2a, the fitness map intercepts the ecology map on its lower stable branch, thus predicting a stable eco-evolutionary
equilibrium of low density and intermediate toxicity. Figure 2bd illustrates the destabilisation, and potential re-stabilisation of
the original eco-evolutionary equilibrium as caused by the emergence of a public good. This may happen through shifts in the
ecology map (Fig. 2b), the fitness map (Fig. 2c), or both (Fig. 2d), thus relocating the fitness map in between the two stable
branches of the ecology map. Following destabilisation, higher toxicity evolves (private good of Step 1 in the emergent public
goods sequence) whilst the population density increases modestly, thus remaining in the low density state. At some critical
threshold of toxicity, the low-density equilibrium becomes unstable and the system shifts to its alternate ecological stable state
(high density; positive feedback of Step 2). At high density, there is now selection against toxicity (public good of Step 3),
which leads eventually to the collapse of the population on to its original (low density) ecological state, with reduced toxicity
(tragedy of the commons of Step 4). A similar type of eco-evolutionary hysteretic cycle was first described by Dercole et al.
(2002) in a different biological context (evolution of body size in a competitive system).
Figure 2 emphasises that each of these shifts may be caused by some environmental perturbation. In Figure 2b, the environmental perturbation moves the ecology map upward; this might be the result of some nutrient input, which would cause an
increase in density independently of the trait value, or circulation patterns that cause the formation of dense cell aggregations.
In Figure 2c, the environmental perturbation moves the fitness map upward, as a consequence of selection becoming more
favourable to toxicity at low density. This might be caused by increased densities of prey, such as soft-bodied algae. This change
causes higher competition for inorganic nutrients, but simultaneously results in greater availability of organic nutrients derived
from intraguild predation. Both changes favour increased reliance on toxin-mediated predation. Because shifts in the ecology
and/or fitness maps may not be permanent, the system is predicted to return to its original eco-evolutionary equilibrium as the
effects of the environmental perturbation dissipate. This might occur at various points along the cycle, thus potentially generating a rich array of bloom dynamics, varying notably in their duration and toxicity at the onset of the termination phase.
Finally, Figure 2e and f underscore that the existence of alternate stable ecological states is not strictly required. In Figure 2f,
both the ecology and fitness maps are destabilised, causing the replacement of the original eco-evolutionary equilibrium with a
stable limit cycle. Steps 14, however, still apply to the four different phases of the cycle (increase in toxicity, increase in
density, decrease in toxicity and decrease in density).
(Teegarden et al. 2001; Vanderploeg et al. 2001). Indeed,

introduced (Schoenberg & Carlson 1984) and native (Wang
et al. 2010) selective predators can promote the growth of
toxic cyanobacteria in natural communities, underscoring the

potential for the indirect effects of selective predation to
facilitate TABs.
Table 1 Studies that have demonstrated cell- or colony-level advantages of toxicity
Toxic alga
Defence
Cyanobacteria
Dinoflagellate
Haptophyte
Heterokontaphyte
Predator
Microcystis sp.
Nodularia spumigena
Alexandrium fundyense
Alexandrium sp.
Alexandrium minutum
Karenia mikimotoi
Emiliania huxleyi
Heterosigma akashiwo
Toxic alga
Offence
Dinoflagellate
Haptophyte
Heterokontaphyte
References
Native zooplankton
Mollusc
Cladoceran
Copepods
Arthropod
Copepods
Copepod
Copepods
Microbial predators
Dreissena polymorpha
Bosmina longirostris
Various
Acartia hudsonica
Three species
Acartia tonsa
Two species
Various
Various
Prey
Alexandrium pseudogonyaulax
Karlodinium veneficum
Prymnesium parvum
Chattonella ovata
Wang et al. (2010)

Vanderploeg et al. (2001);Raikow et al. (2004)
Schoenberg & Carlson (1984)
Gorokhova & Engstrom-Ost (2009)
Colin & Dam (2003)
Teegarden (1999)
Selander et al. (2006)
Schultz & Kirboe (2009)
Strom & Bright (2009)
Graham & Strom (2010)
Reference
Various microalgae
Microalga
Microalga
Cyanobacteria
Storeatula major
Dunaliella tertiolecta
Synechococcus
Blossom et al. (2012)

Sheng et al. (2010)
Driscoll et al. (2013)
Jeong (2011)
References are available in Supplemental Materials.
prey prior to ingestion (Sheng et al. 2010). Another dinoflagellate, Alexandrium pseudogonyaulax, secretes extracellular
toxic mucous traps that facilitate predation by snaring motile
prey (Blossom et al. 2012). The haptophyte Prymnesium parvum kills prey following a relatively brief period of direct contact, and then engulfs the lysed material (Driscoll et al., in
prep). Finally, cells of two raphidophytes excrete toxic
mucous bodies, which remain bound to the cell surface (Yamasaki et al. 2009) and snare small, live prey prior to ingestion (Jeong 2011).
Toxin-mediated predation suggests a plausible private
benefit of toxin production, even when toxic cells are rare. Just
as predators of chemically defended microalgae vary in their
selectivity, the degree to which offensive toxicity is incentivized
at the cell-level will depend on the abundance of suitable prey.
Toxic mixotrophs vary widely in their prey specificity, and may
be limited by the size (Hansen & Calado 1999) or physical
defences of prey, even when prey may be killed. The rigid, siliceous frustule of diatoms in particular appears to prevent phagocytosis by the otherwise omnivorous dinoflagellate Karlodinium
armiger (Berge et al. 2008) and haptophyte P. parvum (Tillmann 1998; Driscoll et al. 2013). However, in sufficient densities, both of these species employ collective wolf pack
Table 2 Evidence that direct cell contact is required for toxicity
Toxic alga
Dinoflagellate
Haptophyte
Method
References
Pfiesteria
Heterocapsa
Membrane
Filtrate
Karenia
Cochlodinium
Karlodinium
Prymnesium
Membrane
Membrane
Filtrate
Membrane;
filtrate
Vogelbein et al. (2002)

Uchida et al. (1995);
Yamasaki et al. (2011)
Zou et al. (2010)
Berge et al. (2012)
Remmel & Hambright
(2012)

strategies of predation upon larger organisms, including animals (Berge et al. 2012; Remmel & Hambright 2012).
From cell- to community-level effects
Toxic algae blooms have long been viewed as the outcome

of population-scale adaptive strategies, requiring the concerted efforts of billions of cells. According to this view,
the primary ecological benefits responsible for the evolution
of toxigenesis are the cooperative elimination of competitors
(allelopathy) and predators (grazer killing). Objections to
the tendency to view toxicity as cooperation have been
raised fairly regularly over the past three decades (e.g.
Lewis 1986; Thornton 2002; Jonsson et al. 2009). In fact, if
cell- or colony-level selection is sufficient to favour toxicity
through direct trophic interactions, many of the most conspicuous ecological benefits associated with blooms are
byproducts from an evolutionary standpoint. For example
toxins that deter selective predators (Teegarden 1999;
Guisande et al. 2002) may, in sufficient densities, kill
(Barreiro et al. 2006) or impair (Teegarden et al. 2008)
predators that do not discriminate among toxic and nontoxic prey. Similarly, lytic chemicals that facilitate intraguild
predation can kill even those competitors which may not be
consumed (Driscoll et al. 2013) or suppress predators of the
toxic population (Adolf et al. 2007; Waggett et al. 2008).
Thus, multiple novel ecological benefits may emerge beyond
threshold cell concentrations of toxic cells (Fig. 3), potentially leading to positive feedbacks between density and net
growth (Irigoien et al. 2005; Sunda et al. 2006).
The transition from relatively subtle, cell-level private functions of toxicity to conspicuous, community-scale public good
benefits frequently depends on threshold densities of toxic
cells. The dinoflagellate Karlodinium armiger and haptophyte
Prymnesium parvum can be safely consumed by animal and
microbial predators at low densities; however, beyond threshold concentrations, the trophic interaction reverses, and the
(a)
(b)
(c)
Figure 3 Examples of transitions from private advantages to public goods. (a) Toxins evolved to immobilise and kill prey may poison predators when toxic
cells are sufficiently abundant. (b) Toxins that assist in predation may also act as allelochemicals when they target non-prey competitors. (c) Toxins that
defend individual cells or colonies by dissuading selective predators may impair or kill indiscriminate predators at sufficient densities.
microalgae kill and feed upon their predators (Tillmann 2003;

Berge et al. 2012). Although these direct interactions may benefit the individual cells involved, there are nevertheless broader
beneficial impacts not only for conspecifics, but for all (resistant) potential prey of the killed predators. A similar transition
may occur simply via changes in abundances of different
predators. For example individual colonies of toxic cyanobacteria benefit through toxin production when predators are capable of avoiding or rejecting toxic colonies (Table 1); however,
their negative effects on indiscriminate predators following
ingestion can only benefit all remaining potential prey, including non-toxic populations (Table 2; Figure 1c).
Dense, highly toxic populations may also harm

heterospecific populations that (directly or indirectly) benefit
toxic lineages. Susceptible prey populations provide direct
benefits to individual toxic predators, but are unlikely to
persist at appreciable densities during ecosystem-disruptive
blooms of their predators (Adolf et al. 2008). Similarly,
even highly selective predators may suffer at extreme toxic
population frequencies or densities (Vanderploeg et al.
2009). Loss of susceptible prey and selective predators
would remove agents of selection favoring toxin production
at the cell-level for offensive and defensive functions, respectively.
Table 1 Studies that have demonstrated cell- or colony-level advantages of toxicity
Toxic alga
Defence
Cyanobacteria
Dinoflagellate
Haptophyte
Heterokontaphyte
Predator
Microcystis sp.
Nodularia spumigena
Alexandrium sp.
Alexandrium minutum
Karenia mikimotoi
Emiliania huxleyi
Toxic alga
Offence
Dinoflagellate
Haptophyte
Heterokontaphyte
References
Native zooplankton
Mollusc
Cladoceran
Copepods
Arthropod
Copepods
Copepod
Copepods
Microbial predators
Dreissena polymorpha
Bosmina longirostris
Various
Acartia hudsonica
Three species
Acartia tonsa
Two species
Various
Various
Prey
Alexandrium pseudogonyaulax
Prymnesium parvum
Chattonella ovata
Wang et al. (2010)

Vanderploeg et al. (2001);Raikow et al. (2004)
Schoenberg & Carlson (1984)
Gorokhova & Engstrom-Ost (2009)
Colin & Dam (2003)
Teegarden (1999)
Selander et al. (2006)
Schultz & Kirboe (2009)
Strom & Bright (2009)
Graham & Strom (2010)
Reference
Various microalgae
Microalga
Microalga
Cyanobacteria
Storeatula major
Dunaliella tertiolecta
Synechococcus
Blossom et al. (2012)

Sheng et al. (2010)
Jeong (2011)
prey prior to ingestion (Sheng et al. 2010). Another dinoflagellate, Alexandrium pseudogonyaulax, secretes extracellular
toxic mucous traps that facilitate predation by snaring motile
prey (Blossom et al. 2012). The haptophyte Prymnesium parvum kills prey following a relatively brief period of direct contact, and then engulfs the lysed material (Driscoll et al., in
prep). Finally, cells of two raphidophytes excrete toxic
mucous bodies, which remain bound to the cell surface (Yamasaki et al. 2009) and snare small, live prey prior to ingestion (Jeong 2011).
Toxin-mediated predation suggests a plausible private
benefit of toxin production, even when toxic cells are rare. Just
as predators of chemically defended microalgae vary in their
selectivity, the degree to which offensive toxicity is incentivized
at the cell-level will depend on the abundance of suitable prey.
Toxic mixotrophs vary widely in their prey specificity, and may
be limited by the size (Hansen & Calado 1999) or physical
defences of prey, even when prey may be killed. The rigid, siliceous frustule of diatoms in particular appears to prevent phagocytosis by the otherwise omnivorous dinoflagellate Karlodinium
armiger (Berge et al. 2008) and haptophyte P. parvum (Tillmann 1998; Driscoll et al. 2013). However, in sufficient densities, both of these species employ collective wolf pack
Table 2 Evidence that direct cell contact is required for toxicity
Toxic alga
Dinoflagellate
Haptophyte
Method
References
Pfiesteria
Heterocapsa
Membrane
Filtrate
Karenia
Cochlodinium
Karlodinium
Prymnesium
Membrane
Membrane
Filtrate
Membrane;
filtrate
Vogelbein et al. (2002)

Uchida et al. (1995);
Zou et al. (2010)
Berge et al. (2012)
Remmel & Hambright
(2012)

strategies of predation upon larger organisms, including animals (Berge et al. 2012; Remmel & Hambright 2012).
From cell- to community-level effects
Toxic algae blooms have long been viewed as the outcome

of population-scale adaptive strategies, requiring the concerted efforts of billions of cells. According to this view,
the primary ecological benefits responsible for the evolution
of toxigenesis are the cooperative elimination of competitors
(allelopathy) and predators (grazer killing). Objections to
the tendency to view toxicity as cooperation have been
raised fairly regularly over the past three decades (e.g.
Lewis 1986; Thornton 2002; Jonsson et al. 2009). In fact, if
cell- or colony-level selection is sufficient to favour toxicity
through direct trophic interactions, many of the most conspicuous ecological benefits associated with blooms are
byproducts from an evolutionary standpoint. For example
toxins that deter selective predators (Teegarden 1999;
Guisande et al. 2002) may, in sufficient densities, kill
(Barreiro et al. 2006) or impair (Teegarden et al. 2008)
predators that do not discriminate among toxic and nontoxic prey. Similarly, lytic chemicals that facilitate intraguild
predation can kill even those competitors which may not be
consumed (Driscoll et al. 2013) or suppress predators of the
toxic population (Adolf et al. 2007; Waggett et al. 2008).
Thus, multiple novel ecological benefits may emerge beyond
threshold cell concentrations of toxic cells (Fig. 3), potentially leading to positive feedbacks between density and net
growth (Irigoien et al. 2005; Sunda et al. 2006).
The transition from relatively subtle, cell-level private functions of toxicity to conspicuous, community-scale public good
benefits frequently depends on threshold densities of toxic
cells. The dinoflagellate Karlodinium armiger and haptophyte
Prymnesium parvum can be safely consumed by animal and
microbial predators at low densities; however, beyond threshold concentrations, the trophic interaction reverses, and the
Table 4 Evidence for public good benefits of toxicity extending to non-toxic conspecifics or heterospecifics
Toxic microalga
Cyanobacteria
Microcystis aeruginosa
Dinoflagellate
Alexandrium minutum
Alexandrium sp.
Haptophyte
Prymnesium parvum
Target
Benefit
Non-toxic beneficiary
Public good
undermined?
References
Tilapia
Cladoceran
Microbe
Copepod
Native copepod species (4)
Microbe
Copepod
Co-occurring centric diatom
P
P
P
P
P
P
P
C
Conspecific
Conspecific
Conspecific
Conspecific
Heterospecific
Conspecific
Conspecific
Conspecific
Yes
Yes
No
Yes
n.d.
Yes
Yes
Yes
Keshavanath et al. (1994)

Van Gremberghe et al. (2009)
John et al. (2014)
Barreiro et al. (2006)
Teegarden et al. (2008)
Adolf et al. (2007)
Waggett et al. (2008)
P is reduced predation pressure; C is reduced competition. References are available in Supplemental Materials.
subsequent years (Briand et al. 2005). The variation in the

eco-evolutionary patterns of these populations is in some ways
unsurprising, considering the many potential direct and
indirect effects of toxigenesis in this group, as well as the
potential for coevolution with important predators (see Coevolution and the fate of blooms below). Blooms formed by
Alexandrium fundyense in a closed off salt marsh were highly
divergent from an adjacent coastal bloom, and showed extremely fast genetic turnover (populations differentiated in as
little as 7 days) (Richlen et al. 2012). Rapid adaptation is
again a likely explanation, but information about phenotypic change will naturally be required to identify agents of
selection.
Is the tragedy of the commons relevant to TABs?
The final stage in the emergence of a public good is the tragedy of the commons (Hardin 1968), in which exploitation of
the benefits of toxicity by non-producers results in the deterioration of the public good. This intriguing possibility is
relatively unexplored in the TAB literature, at least as it
pertains to intraspecific variation in toxigenesis. We explore
the possibility of cheating with respect to the two basic
large-scale public goods that may emerge from the success of
toxic lineages: impairment/killing of predators, and allelopathy. In both cases, substantially more work has focused on
interspecific effects, probably due to technical challenges with
tracking the dynamics of genotypes (compared with distinct
species) or a tendency to view toxic populations as functionally homogeneous (Burkholder & Glibert 2006). Nevertheless,
exploitation of emergent public goods by heterospecifics
reflects a conceptually similar ecological (rather than evolutionary) path to the tragedy of the commons.
Researchers have long recognised the important roles of
non-toxic prey for the feeding behaviour and health of predators exposed to toxic prey. Non-toxic prey may have two
contrasting (but not necessarily mutually exclusive) impacts
on predators, which ultimately impact the toxic population in
opposite ways. Selective predators may target non-toxic prey
when available, but consume toxic prey in the absence of nontoxic alternatives. Alternatively, non-toxic algae may have a
positive effect on the health of indiscriminate predators, which
consume both toxic and non-toxic prey. Selective predators
are frequently observed in TABs (and may actually contribute
to their formation and persistence), whereas indiscriminate,
high-throughput feeders like Daphnia may be capable of controlling relatively sparse toxic populations precisely because
they (typically) do not avoid toxic lineages (Schoenberg &
Carlson 1984; Gobler et al. 2007). Thus, if non-toxic prey is
able to increase to sufficient densities within a TAB, they may
compromise the public good of protection from indiscriminate predators and even facilitate the re-emergence of these
important populations (Schoenberg & Carlson 1984).
Although laboratory experiments have demonstrated this
effect to various degrees and over limited scales, we are
unaware of field studies that have deliberately manipulated
the relative abundances of toxic and non-toxic prey.
Even less is known about the potential for non-toxic,
resistant populations to undermine the competitive advantage conferred by allelopathy. Because allelopathy necessarily requires that toxins have broad-spectrum impacts on cooccurring microalgae, this particular benefit is most likely to
assist producers of offensive toxins. (However, we note
that lytic toxins produced by predatory algae may nevertheless be harmful to predators of these species (John et al.
2002, 2014)). In at least two cases, non-toxic lineages isolated from TABs formed by predatory taxa showed distinct
preference for autotrophic growth (Bachvaroff et al. 2009;
Driscoll et al. 2013); however, TAB-forming mixotrophs are
typically poor competitors for inorganic nutrients (Burkholder et al. 2008). It is possible that a preference for
autotrophic growth (and corresponding reduction in toxicity)
following reductions in prey populations and extinction of
most autotrophic competitors represents a short-term (and
short-sighted) adaptation to TAB conditions. Although one
study found limited evidence that a non-toxic subpopulation
undermined allelopathy as an emergent public good (Driscoll et al. 2013), more work is needed to test this prediction
in this and other taxa.
Interestingly, many TABs formed by allelopathic species
harbor significant populations of heterospecific microalgae
(Michaloudi et al. 2009; Hakanen et al. 2014; PoulsonEllestad et al. 2014), and co-culture tests have found that
co-occurring heterospecifics may be resistant to TAB-forming
populations (Hakanen et al. 2014; Poulson-Ellestad et al.
2014). Such non-toxic, resistant populations have the potential
to compete directly with allelopaths, partially nullifying this
emergent benefit (Chao & Levin 1981; Durrett & Levin 1997).
Furthermore, if these lineages reduce the allelopathic potential
of the population, it is possible that they might compromise
the low-competition public good established by their toxic

competitors and provide a window of opportunity for susceptible populations to become re-established. These observations
underscore the ecological (as well as evolutionary) instability
of emergent public goods within diverse, unstructured
communities (Fig. 4).
Abiotic processes are well known to play central roles in
the initiation, persistence, and termination of TABs, often by
magnifying or ameliorating the ecological effects of toxigenic
populations. For example eutrophication permits explosive
growth of autotrophs, but selective predators are likely
responsible for the rise of toxic lineages in particular
(Schoenberg & Carlson 1984; Gobler et al. 2007; Wang et al.
2010). Hydraulic processes can trigger or disrupt blooms by
concentrating or diluting toxic populations (Schwierzke-Wade
et al., 2010), respectively, thus quickly moving the population
above or below key thresholds for novel ecological benefits
(e.g. reduced predation and competition). The accumulation
of non-toxic conspecifics may work in concert with wellrecognised mechanisms (e.g. hydraulic flushing, nutrient
depletion) to facilitate the re-establishment of important, susceptible populations. This possibility remains almost entirely
unexplored, and has the potential to inform novel, environmentally benign bloom remediation strategies.
SYNTHESIS: WHAT CAN TOXIC ALGAL BLOOMS

TEACH US ABOUT ECO-EVOLUTIONARY FEEDBACKS
IN NATURE?
Toxic blooms result from a positive feedback between cell

density and population growth. Together with individual-level
selection for toxicity at low cell density, environmental factors
that cause local increases in density (e.g. aggregation due to
currents; eutrophication) may be required to drive the population across a threshold of total toxicity. Novel ecological
effects of toxins then accumulate as densities rise, including
the destruction or suppression of natural enemies within the
plankton community. The dieback of key susceptible populations (or the rise of resistant lineages), particularly potential
prey and predators of the toxic population, may relax celllevel selection for toxicity. The concurrent accumulation of
widely distributed benefits of toxigenesis and removal of
agents of selection for toxicity operating at the cell-level may
then result in the emergence of a massive public goods game.
The basic elements of this hypothesis are intended to be
quite general and may, in principle, be applied to both aquatic
and terrestrial ecosystems. Indeed, TABs are formed by a
deeply divergent group of prokaryotes and eukaryotes, despite
the many profound differences in toxins and eco-physiology
(c)
(d)
(b)
(a)
Figure 4 Schematic representation of eco-evolutionary feedback during a TAB. (a) Under non-bloom conditions, toxin production is favoured by selection
at the cell-level (private good). (b) Localised increases in toxic cell density, through growth, aggregation or physical concentration, trigger the emergence of
large-scale ecological advantages, which re-structure the community (positive feedback). (c) In the absence of cell-level agents of selection that favour toxin
production, non-toxic, resistant lineages (potentially including conspecific and heterospecific lineages) invade the bloom (public good). (d) Bloom
termination may be triggered by a variety of factors, including exogenous (e.g. changes in temperature), endogenous (e.g. decreased toxicity; tragedy of the
commons), or complex interactions of many factors (e.g. hydraulic flushing and diminished toxicity permit re-establishment of susceptible community).
that separate these species. Propensity to form TABs may

therefore result from different toxin-mediated ecological
strategies (including defensive and offensive) employed by
evolutionarily distant taxa. Might the patterns and processes
that underlie TAB formation transcend the aquatic/terrestrial
divide?
Emergent public goods in terrestrial and laboratory systems
Evidence from a variety of natural and laboratory systems

suggests that many important traits may vary (continuously
or more discretely) between exclusively benefiting the individuals that express them and helping a broader set of beneficiaries. Whether a trait represents an investment in the private
or public good may be determined by the frequency or
density of bearers, the physical environment, interactions with
other members of the community, or various combinations of
these factors. Although the notion of public goods is most
frequently associated with conspicuous extra-organismal investments (e.g. secreted products, constructed habitats), it is
actually the spatial extent of the beneficial effects of a trait
that defines its position along the private-to-public continuum.
Below, we briefly summarise well-studied illustrations of key
aspects of emergent public goods from terrestrial plant
communities, animal predatorprey interactions and laboratory microbial communities, before returning to the question
of TABs as model systems for the broader study of ecoevolutionary feedbacks.
Terrestrial plant communities: public goods arise from indirect
interactions
Ecologists have long recognised the potential for plants to

influence one another indirectly via their direct interactions
with animals, fungi, and microbes, which may spill over to
impact neighbours. The specific effect on neighbours naturally
depends on the nature of the interaction: a palatable neighbour may be helpful or harmful, depending on whether it
attracts herbivores over small (inter-individual) or large (interpatch) scales; the inverse is true of unpalatable neighbours.
Thus, a palatable species may benefit from reduced grazing
pressures in the presence of a heterospecific that invests heavily in defence chemicals, if grazers select among patches
rather than individual plants (Ruttan & Lortie 2015). Similar
potentials exist for neighbour-mediated effects when volatile
compounds signal herbivore attack (Dolch & Tscharntke
2000) or summon carnivorous bodyguards that benefit plants
by attacking herbivores (Dicke & Baldwin 2010).
Costly traits involved in influencing interspecific interactions
may benefit neighbouring conspecifics, which may or may not
invest in these same traits. This possibility has been studied in
the context of defences against herbivores, as well as the
production of competitive compounds that harm interspecific
competitors. Two examples of such indirect intraspecific interactions involve polymorphisms in conspicuous defences
against insect herbivores: the bent candy cane stem of the
tall goldenrod (Solidago altissima; (Wise 2009)), and the production of trichomes resulting in a hairy phenotype in Arabidopsis halleri (Sato et al. 2014; Sato & Kudoh 2015). In
both cases, the defensive phenotype conferred herbivore resistance for rare plants in the presence of high proportions of
undefended plants, consistent with a private good. However,
defended plants gained additional benefits at a patch level
when surrounded by high frequencies of other defended
plants. Furthermore, both studies found evidence that undefended plants may enjoy reduced herbivory in patches dominated by defended plants (although not to the same extent as
defended individuals), consistent with defence as a partially
privatised public good (Wise 2009; Sato et al. 2014).
The spatial scales over which the benefits of plant defences
accrue depend on the dominant herbivore(s), which may vary
dramatically in selectivity, motility, generation time, and tolerance. Most evidence that the benefits of chemical defences can
extend to undefended heterospecific neighbours has come
from studies that focus on large mammalian herbivores (see
Ruttan & Lortie 2015 and references therein). In contrast,
insect herbivores are generally expected to be more selective
over local scales, shifting the scale of benefits towards the
individual-level (Ruttan & Lortie 2015), consistent with a
private good. In fact, the patch-level benefits of trichomes
depends on the specific insect herbivore: although a flightless
beetle and butterfly both preferentially grazed undefended
plants, the patch-level benefits of defence were only observed
in the slow-moving flightless beetle (Sato & Kudoh 2015).
Thus, the balance between private and public benefits of
defensive adaptations may shift with the abundance and
activity of functionally distinct herbivores, as well as local
abundance of defended plants. Based on the relatively few
empirical studies that have addressed these issues, it appears
that (1) defended plants can gain a relative fitness advantage
when rare, or when selective herbivores dominate; (2) high frequencies of defended plants may benefit all plants within a
patch (although this pattern depends on herbivores), and (3)
undefended plants may benefit from growth near high densities of defended conspecifics. Whether and to what extent (4)
regional abundances of different herbivores can be driven by
frequencies of defended plants remains, to our knowledge,
unknown.
Many plants employ secreted toxins that suppress
heterospecific competitors (allelopathy). Different genotypes
of the black mustard (Brassica nigra) invest to different
degrees in sinigrin production, which (among other effects)
inhibits heterospecific competitors without impacting conspecifics (Lankau 2008). High sinigrin producers out-perform
a low-producing lineage during invasion of established
heterospecific communities and were more resistant to invasion by heterospecifics; however, low-producers excelled in
intraspecific competition (Lankau & Strauss 2007). Indeed,
the sign of selection on sinigrin content reversed between communities in which B. nigra was rare or common, favouring
reduced sinigrin levels as B. nigra densities increase (Lankau
& Strauss 2007). Finally, allelochemicals are partly responsible
for the success of the invasive plant Alliaria petiolata within
native communities in North America; however, the competitive ability of these populations deteriorates over time due to
selection for reduced allelochemical production (Lankau et al.
2009). Thus, (1) allelochemical production yields advantages
to individual plants when invading communities dominated by
susceptible heterospecifics, (2) high patch-level allelochemical

production suppresses heterospecific invaders, (3) selection
favours reduced investment in allelochemicals when conspecifics are common (and heterospecifics rare), and (4) population-level competitive ability is undermined by decreasing
investment in allelochemicals.
Individual- and group-level advantages of chemical defences in
animals
Many insects have evolved defensive endotoxins that discourage predation. However, this mode of defence requires that
the predator taste the prey, which frequently results in injury
or death to the prey before the predator can change its
behaviour. As a result, defensive toxins are frequently
accompanied by visual warning signals, which allow experienced predators to avoid toxic prey altogether. In this scenario, a few toxic animals benefit conspecifics by teaching
predators to avoid similar individuals. However, non-toxic
prey may evolve to mimic these signals, potentially compromising the reliability of the signal in the eyes of the predator.
The potential private (individual-level) and public (grouplevel) advantages of chemical defences have been investigated
experimentally using birds as model predators. Skelhorn &
Rowe (2007) found that non-defended prey models were
preferentially consumed as they became more common relative to defended prey, whereas Jones et al. (2013) found that
rising local frequencies of non-toxic mimics resulted in higher
predation rates for all targets, regardless of defence. A recent
experiment by Speed et al. (in prep) neatly captured both private and public benefits of defence: survival following initial
attacks is largely dictated by individual-level defensive status,
whereas initial attack rates decrease for all prey when
defended insects are locally common. Thus, (1) defence may
improve individual-level survival regardless of neighbour
strategies, (2) local attack frequencies decline with increased
proportions of defended prey, (3) undefended prey experience
reduced attack rates in otherwise well-defended groups, and
(4) rising frequencies of undefended prey may (or may not)
increase local attack frequencies for all phenotypes.
from invertase produced by others (Greig & Travisano 2004).

Non-producers can gain a relative fitness advantage when
grown with high densities of producers in structured (Greig &
Travisano 2004) and unstructured (Gore et al. 2009) environments. However, producers enjoy direct fitness advantages in
sparse populations (Greig & Travisano 2004; Gore et al. 2009).
Thus, the degree to which benefits of production are localised
to producer cells is determined by their density; however, densities can drop as non-producers accumulate, consistent with a
tragedy of the commons (Sanchez & Gore 2013). Together,
these results show that (1) individual producers privatise the
benefits of production in sparse populations; (2) population
density increases with the proportion of producers; and (3)
non-producers exploit invertase produced by others in dense
populations, ultimately (4) undermining the public good and
causing population declines. These ingredients yield a full ecoevolutionary feedback that closely approximates the snowdrift
game, which allows stable coexistence between producers and
non-producers (Sanchez & Gore 2013; Box 2).
The formation of multicellular aggregates or colonies is a general defence against predation by relatively small, gape-limited
predators, and is common among microbial taxa. In the unicellular green alga, Chlamydomonas reinhardtii, predation by the
small rotifer Brachionus calyciflorus resulted in the rapid
appearance of palmelloids [small, matrix-encased colonies;
(Becks et al. 2010)]. Palmelloid production was heritable (i.e.
not inducible, as is the case in many microalgae), and resulted
in resistance to grazing at a cost of reduced intraspecific competitive ability. In mixed cultures, rotifers preferentially consumed unicells, leading to accumulation of inedible palmelloids.
Rotifer populations then dropped sharply due to starvation,
relaxing selection against unicells. Finally, the rapid accumulation of unicells under relaxed grazing pressures led to the recovery of the rotifer populations (Becks et al. 2010). Therefore, (1)
palmelloid formation confered advantages in the presence of
heavy predation pressure, (2) high proportions of palmelloids
led to predator starvation, relaxing predation pressures for the
entire population, (3) unicellular lineages out-competed palmelloid-forming neighbours within the newly established lowpredation environment, and (4) the rise of unicells triggered the
recovery of rotifer populations.
Ecologically driven switches between private and public goods in

laboratory microbes
Why dont terrestrial ecosystems face toxic blooms?
The past decade has seen a rapid increase in the attention

paid to microbial social behaviours, particularly those mediated by secreted metabolites. The term public good is frequently used to refer to these beneficial, extracellular
products, based on the assumption that individual producers
cannot privatise the positive effects of extracellular products
(K
ummerli & Ross-Gillespie 2013). However, there is
mounting evidence that secreted products may yield relative
fitness advantages to producing bacteria in the presence of
non-producing lineages, consistent with a private good (Zhang
& Rainey 2013; Scholz & Greenberg 2015).
Some strains of brewers yeast (Saccharomyces cerevisiae)
secrete invertase, an enzyme that digests sucrose into glucose
and fructose, which may then be taken up by cells. However,
some strains do not produce invertase, and are able to benefit
Despite the evidence that emergent public goods may be

important in terrestrial plant and animal communities, TABs
appear to lack obvious terrestrial analogues. Certainly, toxins
have evolved for both offensive and defensive functions
among terrestrial microbes and macrobes, and are central to
the ecological success of many members of these groups. Furthermore, certain elements of TABs may find limited parallels
in plants and animals; for example bark beetle outbreaks
amplify via a positive feedback mediated transition from
targeting small prey at low densities, to indiscriminately
overwhelming even the largest and healthiest trees at high
densities (Boone et al. 2011). Invasive plants (particularly
those that employ allelopathy) can rapidly rise to great densities at the expense of native, susceptible communities (Lankau
2012). Yet, from the perspective of the focal organisms them-
selves, none of these phenomena appear to match TABs in

terms of spatio-temporal extent or disruptive power across the
functional spectrum of a native community.
It is crucial to delineate the relevant differences between
aquatic and terrestrial communities to appreciate the unique
possibilities for eco-evolutionary feedbacks to shape TAB
dynamics, and to critically assess the utility of TABs as natural laboratories for the study of such dynamics. After all, a
useful model system should offer unique features that are
practically advantageous, without obviously setting it apart
from the less accessible systems that it is intended to model.
We therefore highlight key distinctions between aquatic
(planktonic) systems and their terrestrial (mostly sessile)
counterparts. We focus on those differences with the most
direct relevance to the occurrence of TAB-like phenomena,
to the exclusion of many other interesting distinctions that
fundamentally alter the ways in which ecology and evolution
play out on land and in water.
(1) The relative importance of top-down vs. bottom-up
controls on standing photosynthetic biomass. Herbivores
consume far more primary productivity in aquatic than
terrestrial environments (Cyr & Face 1993; Shurin et al.
2006). As a result, the fraction of net primary productivity
accounted for by standing photosynthetic biomass is estimated to be two orders of magnitude lower in aquatic than
terrestrial environments (Polis 1999). Terrestrial plant
communities are thus more likely to be limited by bottomup controls on growth (e.g. light, space, nutrients). As a
result, the local success of anti-herbivore defences may
have only a minimal impact on standing biomass. In contrast, microalgae populations are typically maintained far
below their potential, as defined by bottom-up controls.
Thus, even temporary reductions in grazing rates in a particular locale (or upon a particular lineage) can lead to
dramatic increases in standing biomass before bottom-up
controls on algae growth take effect.
(2) Mixotrophs are the ultimate resource generalists. Many
bloom-forming microalgae are capable of exploiting
organic and inorganic nutrients, including particulate
material derived from detritus or live prey (Burkholder
et al. 2008). This nutritional flexibility allows mixotrophs to avoid (or reduce) reliance upon other populations or processes. Although terrestrial animals vary
in their degree of specialisation upon different
resources, all must depend on other species to supply
energy (at a minimum). This reliance ultimately limits
the success of any single population, particularly when
exploitation reduces the ability of a favoured resource
to regenerate (as in the case of living resources). Multichannel or subsidised omnivores are less strongly
coupled to any one resource, and thus are able to
reduce such limitations to some degree (Polis & Strong
1996). Although land plants are less obviously limited,
their reliance upon inorganic nutrients renders them
dependent on heterotrophic communities for nutrient
cycling. In contrast, mixotrophic algae may be almost
entirely self-reliant for energy production, biosynthesis

and nutrient cycling.5
(3) Random and non-random fluid flow can quickly destroy
and create spatial structure. Many important aspects of an
individual land plants habitat remain fixed or change
slowly over its lifetime. In contrast, planktonic microalgae
are constantly drifting, swimming, or being moved by
micro-currents, leading to a highly dynamic local environment. As a result, the conspecific and heterospecific neighbours of a focal, free-swimming microalga can turn over
relatively rapidly. This latter situation more closely
approximates the assumptions of a simple mean field
model, wherein the average competitive environment
experienced by an individual reflects regional densities of
different species. In terrestrial environments, conspecifics
may cluster together due to endogenous (e.g. limited dispersal) or exogenous factors (e.g. patchily distributed
resources). Clustering may limit the success of superior
competitors by increasing the effective (average local) density of conspecifics, thus amplifying intraspecific competition (Chesson 2000). Planktonic communities would seem
to lack this type of cross-generational spatial structure
(although colonial species may be a marginal exception),
thus removing an important mechanism of buffering
communities against invasion by superior competitors,
voracious predators and virulent pathogens.
Occasionally, however, large-scale advection or strong vertical stratification coupled with phototaxis may cause highly
localised accumulations of previously widely dispersed cells.
Such physical processes provide an alternative mechanism of
quickly increasing densities of toxic cells, which does not
involve proliferation. This mechanism appears especially relevant to large, slow-reproducing microalgae that typically exist
in sparse populations (e.g. dinoflagellates).
Together, these differences may help to explain the apparent
restriction of TAB-like phenomena to aquatic systems. However, the radical demographic changes and profound alterations
to community structure that characterise TABs are not required
for the emergence of public goods, or eco-evolutionary feedbacks more broadly. In fact, analogous phenomena may well
play out across a range of terrestrial environments. However,
more rigid population regulation, continuous (rather than discrete) transitions from private to public effects of beneficial
traits, and longer generation times may all serve to minimise
outward evidence of underlying eco-evolutionary processes in
macroscopic communities.
Biological invasions facilitated by allelopathy provide arguably the closest overall terrestrial parallel to the case of TABs.
Although they do not approach the disruptive potential of
TABs across functional groups and trophic levels, invasions
by exotic allelopaths can profoundly impact native communities. Furthermore, the success of invasive populations may
depend largely on costly investments in extra-organismal
compounds, which may function in defensive or competitive
roles. Lankau et al. (2009) found that populations of invasive
annuals invested less in allelochemicals with age (over a scale
5
The authors have observed vigorous populations of P. parvum in vials that
had been neglected for almost two years with no inputs except light.
of decades), which led to declines in the abundances of the

invasive species relative to native competitors. These patterns
are consistent with selection for reduced investment in allelochemicals, despite the importance of this trait for the success
of the population. Furthermore, Lankau (2012) found
evidence that native heterospecific competitors gained resistance to the allelochemicals produced by an invasive plant
over time, allowing them to compete effectively with the
invasive species. Together, these results hint at potentially
deep parallels between invasions of terrestrial ecosystems and
toxic blooms in aquatic environments, underscoring the
possibility for TABs to serve as natural microbial analogues
of important eco-evolutionary dynamics in macroscopic
communities.
Co-evolution and the fate of toxic blooms
Although we have focused primarily on rapid adaptation

within TAB populations, adaptation by other members of
plankton communities in the face of recurrent TABs may
play an important role in bloom dynamics. For example
Daphnia can quickly evolve resistance in response to blooms
of toxic cyanobacteria (Gustafsson & Hansson 2004;
Hairston et al. 2005; Sarnelle & Wilson 2005), restoring its
ability to exert strong top-down controls on toxic cyanobacteria (Chislock et al. 2013). Many TABs harbour significant
populations of apparently resistant heterospecific microalgae
(Michaloudi et al. 2009; Hakanen et al. 2014; Poulson-Ellestad et al. 2014), which are unharmed by exposure to high
doses of toxins in the laboratory (Hakanen et al. 2014;
Poulson-Ellestad et al. 2014).
Resistant heterospecific communities may potentially
control the densities of toxic populations via predation and
competition for nutrients, provided they are able to rise to
significant densities over the course of the bloom. These populations may therefore reduce the duration and severity of
blooms, particularly in environments subjected to regular
TABs, provided that resistant genotypes persist between
bloom seasons. However, the profoundly non-equilibrium
nature of TABs might prevent (or slow) the accumulation of
resistant lineages in native plankton communities, particularly
if resistance imposes costs during non-TAB conditions
(Hairston et al. 2001). It would be interesting to compare coevolution between TAB-forming species and their adversaries
across environments that differ in the regularity with which
TABs occur.
OUTLOOK
The prevalence and importance of eco-evolutionary feedbacks

in nature remains an open question. We have argued that
toxic algal blooms (TABs) are promising candidate natural
laboratories for the study of eco-evolutionary feedbacks in
nature. Our review highlights supporting evidence as well as
open questions and challenges from which the following
research programme can be outlined:
(1) What are the impacts of different environmental perturbations on combined environment and fitness maps? Per 2015 John Wiley & Sons Ltd/CNRS
turbations associated with bloom initiation and

termination may be depicted in an idealised plot of environmental and genetic space, as shown in Box 1. For
instance, transient increases (decreases) of toxic cell concentrations via abiotic processes (e.g. stratification,
hydraulic flushing) may simply increase (decrease) the
elevation of the population, potentially placing it within
the basin of attraction of a new ecological stable state.
Other perturbations are likely to impact both maps; for
instance, nutrient loading may stimulate the growth of
susceptible prey, thus simultaneously increasing population density and selection for toxicity. Theoretical work
will be required to systematically determine the effects of
the different types of perturbation on TAB populations,
and experimental manipulations in the laboratory (i.e.
microcosms) and field (i.e. mesocosms) can be used to
parameterise these models and directly test key predictions.
(2) How do cell-level agents of selection change over the
course of a bloom? There is considerable evidence for
cell-level advantages of toxicity (Table 1); however, these
benefits are rooted in biotic interactions that may be
profoundly impacted by TABs. Key heterospecifics (selective predators and susceptible prey) may decline,
develop resistance or persist throughout blooms. These
divergent ecological and evolutionary responses will
determine the balance of private and public effects of
toxicity, and may thus determine the sign and magnitude
of selection for toxigenesis within TABs. The relevance
of private and public goods can be assessed by observations and manipulations in the field, coupled with laboratory experiments designed to measure the relative
fitness of natural isolates in the presence of different
important heterospecifics.
(3) Do resistant lineages that benefit from TABs contribute
to bloom termination by compromising the public good?
Non-toxic conspecifics and heterospecifics are frequently
isolated from TABs, and in a few cases, these lineages
benefit demonstrably from the presence of toxic strains
(Table 4). Whether these populations act as cheaters
and undermine the collective benefits of toxigenesis
depends on their indirect effects on toxic populations.
The importance of toxicity thresholds (the product of
cell-level toxicity and density of toxic cells) to bloom initiation and collapse suggests that cheaters may play
important and unexplored roles in bloom termination.
To our knowledge, this possibility remains entirely unexplored, but could be tested directly by manipulating initial frequencies of toxic and non-toxic microalgae in
mesocosms or microcosms that re-create salient features
of bloom communities.
The answers to these questions have the potential to inform
research into eco-evolutionary feedbacks more broadly.
Indeed, we have noted some intriguing parallels between
TABs and other important phenomena, including biological
invasions of terrestrial plant communities. The relatively conspicuous, rapid, and easily manipulated dynamics of TABs
may guide future empirical studies of the roles of mutual
interactions between ecological and evolutionary change in

more complex ecosystems. More generally, as we face the
pressing question of the scope and limits of biodiversity and
ecosystem adaptation to global change, there is an urgent
need to better understand the role that eco-evolutionary feedbacks might play in driving catastrophic shifts between alternate ecosystem states. These processes appear to occur
extremely quickly within toxic blooms, providing new opportunities to directly observe these processes as they play out in
natural environments.
ACKNOWLEDGEMENTS
We thank four anonymous reviewers for their help in

improving this manuscript. We would also like to acknowledge helpful comments from K. Foster on an earlier draft of
this manuscript, and discussions with L.L. Sloat, W.C. Adle,
O.T. Eldakar, J.W. Pepper, J.L. Bronstein, A. Dornhaus,
R.E. Michod, S. de Monte, J.-B.Andre and C. Bowler.
W.W.D. was supported by a MemoLife LABEX (ANR10-LABX-54) Postdoctoral Fellowship, NSF IOS-1010669
and NSF ABI-1262472. R.F. acknowledges funding from the
French Centre National de la Recherche Scientifique
(Pepiniere Interdisciplinaire Eco-Evo-Devo de site PSL),
the French Agence Nationale de la Recherche (ANR-09PEXT-011 EVORANGE and ANR-10 PHYTBACK
projects) and the Partner University Fund (collaborative programme Advancing the synthesis of ecology and evolution
between Ecole Normale Superieure and the University of
Arizona).
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SUPPORTING INFORMATION
Additional Supporting Information may be downloaded via

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(www.ecologyletters.com).
Editor, Punidan Jeyasingh

Manuscript received 3 March 2015
First decision made 9 April 2015
Second decision made 25 June 2015
Manuscript accepted 7 September 2015

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Ecology Letters, (2016) 19: 8197

Department of Ecology, Evolution

and Behavior, University of

Department of Ecology and

Evolutionary Biology University of

Eco-evolutionary feedbacks between private and public goods:

Interactions between ecological and evolutionary processes

(Strauss 2014). In particular, the spatial and temporal scales

we highlight major challenges and opportunities within and

Here, we introduce a simple conceptual framework to explain

Although humans have known of toxic algal blooms (TABs)

2015 John Wiley & Sons Ltd/CNRS

Review and Synthesis

the cells, or due to byproduct effects of extreme densities (e.g.

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Private/public goods in eco-evolutionary dynamics 83

Toxicity as chemical defence: deterring choosey predators

Animal and microbial predators4 exert strong top-down

presumably minimising metabolic/physiological costs (Van

Box 1 A graphical model of emergent public goods through eco-evolutionary feedbacks.

Mean trait value

2015 John Wiley & Sons Ltd/CNRS

Review and Synthesis

Response to environmental fluctuation

Mean trait value

(Teegarden et al. 2001; Vanderploeg et al. 2001). Indeed,

toxic cyanobacteria in natural communities, underscoring the

Review and Synthesis

Response to environmental fluctuation

Mean trait value

(Teegarden et al. 2001; Vanderploeg et al. 2001). Indeed,

toxic cyanobacteria in natural communities, underscoring the

Review and Synthesis

Table 1 Studies that have demonstrated cell- or colony-level advantages of toxicity

Wang et al. (2010)

Blossom et al. (2012)

References are available in Supplemental Materials.

Table 2 Evidence that direct cell contact is required for toxicity

Vogelbein et al. (2002)

References are available in Supplemental Materials.

Toxic algae blooms have long been viewed as the outcome

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Private/public goods in eco-evolutionary dynamics 87

microalgae kill and feed upon their predators (Tillmann 2003;

Dense, highly toxic populations may also harm

Review and Synthesis

Table 1 Studies that have demonstrated cell- or colony-level advantages of toxicity

Wang et al. (2010)

Blossom et al. (2012)

References are available in Supplemental Materials.

Table 2 Evidence that direct cell contact is required for toxicity

Vogelbein et al. (2002)

References are available in Supplemental Materials.

Toxic algae blooms have long been viewed as the outcome

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Private/public goods in eco-evolutionary dynamics 89

Keshavanath et al. (1994)

subsequent years (Briand et al. 2005). The variation in the

Review and Synthesis

the low-competition public good established by their toxic

SYNTHESIS: WHAT CAN TOXIC ALGAL BLOOMS

Toxic blooms result from a positive feedback between cell