Documente Academic
Documente Profesional
Documente Cultură
doi: 10.1111/ele.12533
REVIEW AND
SYNTHESIS
William W. Driscoll,1,2,3*
Jeremiah D. Hackett3 and
gis Ferri
Re
ere2,3*
1
INTRODUCTION
82 W. W. Driscoll et al.
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).
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.
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.
84 W. W. Driscoll et al.
Box 1 Continued
Ecological state
(e.g. population size)
(a)
(e)
(c)
(d)
(f)
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).
84 W. W. Driscoll et al.
Box 1 Continued
Ecological state
(e.g. population size)
(a)
(e)
(c)
(d)
(f)
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).
86 W. W. Driscoll et al.
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
Heterosigma akashiwo
Chattonella ovata
Various microalgae
Microalga
Microalga
Cyanobacteria
Storeatula major
Dunaliella tertiolecta
Synechococcus
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
Toxic alga
Dinoflagellate
Haptophyte
Method
References
Pfiesteria
Heterocapsa
Membrane
Filtrate
Karenia
Cochlodinium
Karlodinium
Prymnesium
Membrane
Membrane
Filtrate
Membrane;
filtrate
strategies of predation upon larger organisms, including animals (Berge et al. 2012; Remmel & Hambright 2012).
From cell- to community-level effects
(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.
86 W. W. Driscoll et al.
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
Heterosigma akashiwo
Chattonella ovata
Various microalgae
Microalga
Microalga
Cyanobacteria
Storeatula major
Dunaliella tertiolecta
Synechococcus
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
Toxic alga
Dinoflagellate
Haptophyte
Method
References
Pfiesteria
Heterocapsa
Membrane
Filtrate
Karenia
Cochlodinium
Karlodinium
Prymnesium
Membrane
Membrane
Filtrate
Membrane;
filtrate
strategies of predation upon larger organisms, including animals (Berge et al. 2012; Remmel & Hambright 2012).
From cell- to community-level effects
Table 4 Evidence for public good benefits of toxicity extending to non-toxic conspecifics or heterospecifics
Toxic microalga
Cyanobacteria
Microcystis aeruginosa
Dinoflagellate
Alexandrium fundyense
Alexandrium minutum
Alexandrium sp.
Karlodinium veneficum
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
P is reduced predation pressure; C is reduced competition. References are available in Supplemental Materials.
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
2015 John Wiley & Sons Ltd/CNRS
90 W. W. Driscoll et al.
(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).
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
2015 John Wiley & Sons Ltd/CNRS
92 W. W. Driscoll et al.
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.
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.
94 W. W. Driscoll et al.
REFERENCES
Adolf, J.E., Krupatkina, D., Bachvaroff, T. & Place, A.R. (2007).
Karlotoxin mediates grazing by Oxyrrhis marina on strains of
Karlodinium veneficum. Harmful Algae, 6, 400412.
Adolf, J.E., Bachvaroff, T. & Place, A.R. (2008). Can cryptophyte
abundance trigger toxic Karlodinium veneficum blooms in eutrophic
estuaries? Harmful Algae, 8, 119128.
Bachvaroff, T.R., Adolf, J.E. & Place, A.R. (2009). Strain variation in
Karlodinium veneficum (Dinophyceae): toxin profiles, pigments, and
growth characteristics. J. Phycol., 45, 137153.
Barreiro, A., Guisande, C., Frang
opulos, M., Gonzalez-Fernandez, A.,
Mu~
noz, S., Perez, D. et al. (2006). Feeding strategies of the copepod
Acartia clausi on single and mixed diets of toxic and non-toxic strains
of the dinoflagellate Alexandrium minutum. Mar. Ecol. Prog. Ser., 316,
115125.
Becks, L., Ellner, S.P., Jones, L.E. & Hairston Nelson, N.G. (2010).
Reduction of adaptive genetic diversity radically alters eco-evolutionary
community dynamics. Ecol. Lett., 13, 989997.
Berge, T., Hansen, P. & Moestrup, . (2008). Prey size spectrum and
bioenergetics of the mixotrophic dinoflagellate Karlodinium armiger.
Aquat. Microb. Ecol., 50, 298299.
Berge, T., Poulsen, L.K., Moldrup, M., Daugbjerg, N. & Juel Hansen, P.
(2012). Marine microalgae attack and feed on metazoans. ISME J., 6
(10), 19261936.
Blossom, H.E., Daugbjerg, N. & Hansen, P.J. (2012). Toxic mucus
traps: a novel mechanism that mediates prey uptake in the
mixotrophic dinoflagellate Alexandrium pseudogonyaulax. Harmful
Algae, 17, 4053.
Boone, C.K., Aukema, B.H., Bohlmann, J., Carroll, A.L. & Raffa, K.F.
(2011). Efficacy of tree defense physiology varies with bark beetle
96 W. W. Driscoll et al.
Lankau, R.A., Nuzzo, V., Spyreas, G. & Davis, A.S. (2009). Evolutionary
limits ameliorate the negative impact of an invasive plant. Proc. Natl
Acad. Sci. USA, 106, 1536215367.
Lewis, W.M. (1986). Evolutionary interpretations of allelochemical
interactions in phytoplankton algae. Am. Nat., 127, 184194.
Loret, P., Tengs, T., Villareal, T.A., Singler, H., Richardson, B.,
McGuire, P. et al. (2002). No difference found in ribosomal DNA
sequences from physiologically diverse clones of Karenia brevis
(Dinophyceae) from the Gulf of Mexico. J. Plankton Res., 24, 735739.
Michaloudi, E., Moustaka-Gouni, M., Gkelis, S. & Pantelidakis, K.
(2009). Plankton community structure during an ecosystem disruptive
algal bloom of Prymnesium parvum. J. Plankton Res., 31, 301309.
Nelson, T.A., Lee, D.J. & Smith, B.C. (2003). Are green tides harmful
algal blooms? Toxic properties of water-soluble extracts from two
bloom-forming macroalgae, Ulva fenestrata and Ulvaria obscura
(Ulvophyceae). J. Phycol., 879, 874879.
Paerl, H.W. & Huisman, J. (2009). Climate change: a catalyst for global
expansion of harmful cyanobacterial blooms. Environ. Microbiol. Rep.,
1, 2737.
Polis, G.A. (1999). Why are parts of the world green? Multiple factors
control productivity and the distribution of biomass. Oikos, 86, 3.
Polis, G.A. & Strong, D.R. (1996). Food web complexity and community
dynamics. Am. Nat., 86, 315.
Poulson-Ellestad, K., McMillan, E., Montoya, J.P. & Kubanek, J. (2014).
Are offshore phytoplankton susceptible to Karenia brevis allelopathy? J.
Plankton Res., 36, 13441356.
Rainey, P.B., Desprat, N., Driscoll, W.W. & Zhang, X.X. (2014).
Microbes are not bound by sociobiology: response to K
ummerli and
Ross-Gillespie (2013). Evolution (N. Y)., 6811, 33443355.
Remmel,
E.J.
&
Hambright,
K.D.
(2012).
Toxin-assisted
micropredation:
experimental
evidence
shows
that
contact
micropredation rather than exotoxicity is the role of Prymnesium
toxins. Ecol. Lett., 15, 126132.
Reznick, D.N. (2013). A critical look at reciprocity in ecology and
evolution: introduction to the symposium. Am. Nat., 181, S1S8.
Richlen, M.L., Erdner, D.L., McCauley, L.A.R., Liberal, K. & Anderson,
D.M. (2012). Extensive genetic diversity and rapid population
differentiation during blooms of Alexandrium fundyense (dinophyceae)
in an isolated salt pond on cape cod, MA, USA. Ecol. Evol., 2,
25882599.
Rue, E. & Bruland, K. (2001). Domoic acid binds iron and copper: a
possible role for the toxin produced by the marine diatom Pseudonitzschia. Mar. Chem., 76, 127134.
Ruttan, A. & Lortie, C.J. (2015). A systematic review of the attractantdecoy and repellent-plant hypotheses: do plants with heterospecific
neighbours escape herbivory? J. Plant Ecol., 8, 337346.
Sanchez, A. & Gore, J. (2013). Feedback between population and
evolutionary dynamics determines the fate of social microbial
populations. PLoS Biol., 11, 11e1001547.
Sarnelle, O. & Wilson, A.E. (2005). Local adaptation of Daphnia pulicaria
to toxic cyanobacteria. Limnol. Oceanogr., 50, 15651570.
Sato, Y. & Kudoh, H. (2015). Tests of associational defence provided by
hairy plants for glabrous plants of Arabidopsis halleri subsp. gemmifera
against insect herbivores. Ecol. Entomol., 40, 269279.
Sato, Y., Kawagoe, T., Sawada, Y., Hirai, M.Y. & Kudoh, H. (2014).
Frequency-dependent herbivory by a leaf beetle, Phaedon brassicae, on
hairy and glabrous plants of Arabidopsis halleri subsp. gemmifera. Evol.
Ecol., 28, 545559.
Schoenberg, S.A. & Carlson, R.E. (1984). Direct and indirect effects of
zooplankton grazing on phytoplankton in a hypereutrophic lake. Oikos,
42, 291302.
Schoener, T.W. (2011). The newest synthesis: understanding the interplay
of evolutionary and ecological dynamics. Science, 331, 426429.
Scholz, R.L. & Greenberg, E.P. (2015). Sociality in Escherichia coli:
enterochelin is a private good at low cell density and can be shared at
high cell density. J. Bacteriol., 197, 21222128.
Sheng, J., Malkiel, E., Katz, J., Adolf, J.E. & Place, A.R. (2010). A
dinoflagellate exploits toxins to immobilize prey prior to ingestion.
Proc. Natl Acad. Sci. USA, 107, 20822087.
Shurin, J.B., Gruner, D.S. & Hillebrand, H. (2006). All wet or dried up?
Real differences between aquatic and terrestrial food webs. Proc. Biol.
Sci., 273, 19.
Skelhorn, J. & Rowe, C. (2007). Automimic frequency influences the
foraging decisions of avian predators on aposematic prey. Anim.
Behav., 74, 15631572.
Smallegange, I.M. & Coulson, T. (2013). Towards a general, populationlevel understanding of eco-evolutionary change. Trends Ecol. Evol., 28,
143148.
Stoecker, D.K. (1999). Mixotrophy among dinoflagellates. J. Eukaryot.
Microbiol., 46, 397401.
Strauss, S.Y. (2014). Ecological and evolutionary responses in complex
communities: implications for invasions and eco-evolutionary
feedbacks. Oikos, 123, 257266.
Strom, S., Wolfe, G., Holmes, J., Stecher, H., Shimeneck, C., Lambert,
S. et al. (2003). Chemical defense in the microplankton I: feeding
and growth rates of heterotrophic protists on the DMSproducing phytoplankter Emiliania huxleyi. Limnol. Oceanogr., 48,
217217.
Sunda, W.G., Graneli, E. & Gobler, C.J. (2006). Positive feedback and
the development and persistence of ecosystem disruptive algal blooms.
J. Phycol., 42, 963974.
Teegarden, G.J. (1999). Copepod grazing selection and particle
discrimination on the basis of PSP toxin content. Mar. Ecol. Prog. Ser.,
181, 163176.
Teegarden, G.J., Campbell, R.G. & Durbin, E.G. (2001). Zooplankton
feeding behavior and particle selection in natural plankton
assemblages containing toxic Alexandrium spp. Mar. Ecol. Prog. Ser.,
218, 213226.
Teegarden, G.J., Campbell, R.G., Anson, D.T., Ouellett, A., Westman,
B.A. & Durbin, E.G. (2008). Copepod feeding response to varying
Alexandrium spp. cellular toxicity and cell concentration among natural
plankton samples. Harmful Algae, 7, 3344.
Tester, P.A. & Steidinger, K.A. (1997). Gymnodinium breve red tide
blooms: initiation, transport, and consequences of surface circulation.
Limnol. Oceanogr., 42, 10391051.
Thornton, D.C.O. (2002). Individuals, clones or groups? Phytoplankton
behaviour and units of selection. Ethol. Ecol. Evol., 14, 165173.
Tillmann, U. (1998). Phagotrophy by a plastidic haptophyte, Prymnesium
patelliferum. Aquat. Microb. Ecol., 14, 155160.
Tillmann, U. (2003). Kill and eat your predator: a winning strategy of the
planktonic flagellate Prymnesium parvum. Aquat. Microb. Ecol., 32, 73
84.
Van Dolah, F.M. (2000). Marine algal toxins: origins, health effects, and
their increased occurrence. Environ. Health Perspect., 108(Suppl), 133
141.
Van Donk, E., Ianora, A. & Vos, M. (2011). Induced defences in marine
and freshwater phytoplankton: a review. Hydrobiologia, 668, 319.
Vanderploeg, H.a., Liebig, J.R., Carmichael, W.W., Agy, M.a., Johengen,
T.H., Fahnenstiel, G.L. et al. (2001). Zebra mussel (Dreissena
polymorpha) selective filtration promoted toxic Microcystis blooms in
Saginaw Bay (Lake Huron) and Lake Erie. Can. J. Fish Aquat. Sci., 58,
12081221.
Vanderploeg, H.A., Johengen, T.H. & Liebig, J.R. (2009). Feedback
between zebra mussel selective feeding and algal composition affects
mussel condition: did the regime changer pay a price for its success?
Freshw. Biol., 54, 4763.
Waggett, R., Tester, P. & Place, A. (2008). Anti-grazing properties of the
toxic dinoflagellate Karlodinium veneficum during predatorprey
interactions with the copepod Acartia tonsa. Mar. Ecol. Prog. Ser., 366,
3142.
Wang, X., Qin, B., Gao, G. & Paerl, H.W. (2010). Nutrient enrichment
and selective predation by zooplankton promote Microcystis
(Cyanobacteria) bloom formation. J. Plankton Res., 32, 457470.
Wilson, A.E., Sarnelle, O., Neilan, B.A., Salmon, T.P., Gehringer, M.M.
& Hay, M.E. (2005). Genetic variation of the bloom-forming
Cyanobacterium Microcystis aeruginosa within and among lakes:
implications for harmful algal blooms. Appl. Environ. Microbiol., 71,
61266133.
Wise, M.J. (2009). To duck or not to duck: resistance advantages and
disadvantages of the candy-cane stem phenotype in tall goldenrod,
Solidago altissima. New Phytol., 183, 900907.
Yamasaki, Y., Shikata, T., Nukata, A., Ichiki, S., Nagasoe, S.,
Matsubara, T. et al. (2009). Extracellular polysaccharide-protein
complexes of a harmful alga mediate the allelopathic control it exerts
within the phytoplankton community. ISME J., 3, 808817.
Zhang, X.X. & Rainey, P.B. (2013). Exploring the sociobiology of
pyoverdin-producing pseudomonas. Evolution, 67, 31613174.
SUPPORTING INFORMATION