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Harmful Algae xxx (2013) xxx–xxx

Contents lists available at ScienceDirect

Harmful Algae
journal homepage: www.elsevier.com/locate/hal

Planktonic marine copepods and harmful algae

Jefferson T. Turner a,b,*
a
Biology Department, University of Massachusetts Dartmouth, 285 Old Westport Road, North Dartmouth, MA 02747, USA
b
School for Marine Science and Technology, University of Massachusetts Dartmouth, 706 South Rodney French Boulevard, New Bedford, MA 02744, USA

A R T I C L E I N F O A B S T R A C T

Article history: Marine planktonic copepods are important grazers on harmful algae (HA) species of phytoplankton, and
Received 2 December 2013 copepods are major entry points for vectorial intoxication of pelagic food webs with HA toxins. Previous
Accepted 3 December 2013 reviews (Turner and Tester, 1997; Turner et al., 1998a; Turner, 2006) summarized information on HA
interactions with zooplankton grazers, and vectorial intoxication of pelagic food webs, up through
Keywords: approximately 2005. Accordingly, this review will address primarily studies published during the last
Harmful algae decade. It will concentrate on generic issues in the developing field of HA:grazer interactions, such as the
Copepods
extent to which HA toxins serve as copepod grazing deterrents, induction of HA grazing deterrents by
Dinoflagellates
exposure to copepods, copepod selective feeding to avoid ingesting HA taxa versus non-selective feeding
Zooplankton
Plankton on HA taxa, possible biogeographic aspects of the effects of HA toxins on copepods, impact of copepod
grazing on HA bloom development and termination, the role of copepods as entry points for vectorial
intoxication of pelagic food webs with HA toxins, and possible reasons and remedies for the highly-
variable and conflicting results reported for many studies of copepod grazing on various HA species.
ß 2013 Elsevier B.V. All rights reserved.

1. Introduction Although most earlier studies of zooplankton grazing focused on

Harmful algae (HA) are phytoplankton species that can cause a
variety of deleterious effects in marine ecosystems. Such effects
include production of toxins, with subsequent accumulation and
transport of HA toxins by feeding interactions through benthic and
pelagic marine food webs. In benthic food webs, HA toxins cause
shellfish toxicity in bivalves that ingest toxic HA species. Toxicity
can subsequently cause illness or mortality in humans that
consume intoxicated shellfish. In pelagic food webs HA toxins can
cause vectorial intoxication of upper-trophic-level consumers such
as fish, marine mammals, seabirds and humans. Other effects of
various species of HA include fish kills through direct contact
between fish and water containing certain HA species, anoxia
when large blooms of HA species decompose, and fouling of water
and/or beaches with exudates of some HA species.
Phytoplankton, including HA species, are grazed primarily by
zooplankton. Included are microzooplankton (primarily protists
such as ciliates and heterotrophic dinoflagellates, <200 mm in
longest dimension) and mesozooplankton (metazoans > 200 mm
in longest dimension). The most numerically-dominant compo-
nents of the mesozooplankton are copepods (Schminke, 2007).
* Correspondence to: Biology Department, University of Massachusetts
Dartmouth, 285 Old Westport Road, North Dartmouth, MA 02747, USA.
E-mail address: jturner@umassd.edu
copepods, recent studies over the last two decades suggest that the
largest grazing impact on the phytoplankton, including HA taxa, is
usually by the microzooplankton, not copepods and other
mesozooplankton (Calbet, 2001; Calbet and Landry, 2004; Calbet
et al., 2003; Irigoien et al., 2005; Turner, 2006, 2010). However, HA
toxins have been shown to become concentrated in a variety of
upper-trophic-level pelagic consumers such as fish and marine
mammals, and the entry point for such vectorial intoxication of
pelagic food webs appears to be primarily through copepod
grazing on HA. Thus, this review will focus on interactions between
HA and planktonic copepods.
Previous reviews (Turner and Tester, 1997; Turner et al., 1998a;
Turner, 2006) summarized information on HA interactions with
microzooplankton and mesozooplankton, and vectorial intoxica-
tion of pelagic food webs, up through approximately 2005. Also,
Turner et al. (2002) reviewed information on grazer interactions
with Phaeocystis spp. published prior to 2002, and Nejstgaard et al.
(2007) provided a comprehensive review of studies of zooplankton
grazing on Phaeocystis spp. published through 2006. Accordingly,
this review will address primarily studies published during the last
decade, and the aforementioned reviews should be consulted for
earlier studies. This review will concentrate on generic issues in
the developing field of HA:grazer interactions, such as the extent to
which HA toxins serve as copepod grazing deterrents, copepod
feeding selection against HA taxa versus non-selective feeding on
HA taxa, possible biogeographic aspects of the effects of HA toxins

1568-9883/$ – see front matter ß 2013 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.hal.2013.12.001

Please cite this article in press as: Turner, J.T., Planktonic marine copepods and harmful algae. Harmful Algae (2014), http://dx.doi.org/
10.1016/j.hal.2013.12.001
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2 J.T. Turner / Harmful Algae xxx (2013) xxx–xxx
on copepods, the role of copepods as entry points for vectorial
intoxication of pelagic food webs with HA toxins, and possible
reasons for the highly-variable and conflicting results reported for
many studies of copepod grazing on various HA species.
2. HA taxa
There are >150 species of HA in marine and brackish waters
(Landsberg, 2002), in several algal classes or divisions (Hallegraeff
et al., 2003; Granéli and Turner, 2006). These include Prymnesio-
phyceae (toxic flagellates such as members of the genera
Phaeocystis, Chrysochromulina, and Prymnesium), Raphidophyceae
(toxic golden-brown flagellates of the genera Chattonella, Fibro-
capsa, Heterosigma, and Olisthodiscus), Pelagophyta (brown tide
algae of the genera Aureococcus and Aureoumbra), Cyanophyta
(toxic cyanobacteria), Bacillariophyceae (toxic diatoms of the
genus Pseudo-nitzschia), and Dinophyceae (toxic dinoflagellates).
However, most HA species, particularly those that produce toxins,
are dinoflagellates. Different HA taxa produce a plethora of toxins.
Thus, interactions between copepods and HA taxa are specific for
various combinations of each.
3. HA toxins
There are several different HA toxins which have different
effects on a variety of animals and humans. Toxicity is often
defined by effects on vertebrates that are not direct consumers of
HA, including fish, seabirds, mammals, and humans (Anderson and
White, 1992). Effects of HA toxins on invertebrate zooplankton that
are direct grazers of HA phytoplankton frequently are minimal or
unclear. Thus, whether HA toxins generally function as zooplank-
ton grazing deterrents is unclear.
Most HA toxins affect neurotransmission or inhibit enzymes
(reviewed by Baden and Trainer, 1993; Turner and Tester, 1997;
Turner et al., 1998a). Paralytic shellfish poisoning (PSP) toxins
(collectively known as saxitoxins) produced by dinoflagellates of
the genera Alexandrium (formerly Gonyaulax and Protogonyaulax),
Pyrodinium and Gymnodinium catenatum are water-soluble sodi-
um-ion-channel blockers that progressively inhibit nerve trans-
mission, relaxing smooth muscle and causing paralysis and
respiratory failure in humans, as well as seabirds, fish and marine
mammals. Conversely, brevetoxins produced by the dinoflagellate
Karenia brevis (formerly Gymnodinium brevis, G. breve and
Ptychodiscus brevis) are lipid-soluble sodium-channel activators,
causing repetitive firing of nervous impulses, and resulting
depletion of acetylcholine at synapses. Brevetoxins cause fish kills
by paralyzing the gill muscles of fish on contact. Brevetoxins can
also contaminate shellfish, causing neurotoxic shellfish poisoning
(NSP) in humans. Amnesic shellfish poisoning (ASP) is caused by
the water-soluble amino acid domoic acid (DA), produced by toxic
members of the diatom genus Pseudo-nitzschia. Domoic acid acts as
a surrogate for the excitatory neurotransmitter L-glutamic acid,
and inability to regulate this substitute transmitter causes
extensive neuronal depolarization, particularly in the vertebrate
hippocampus which contains abundant glutamate receptors.
Toxicity due to DA in humans, seabirds and marine mammals
results in brain damage due to degeneration of the hippocampus.
Diarrhetic shellfish poisoning (DSP) is caused by okadaic acid and
several other lipid-soluble toxins produced by some species of the
dinoflagellate genera Dinophysis and Prorocentrum (Yasumoto,
1990). DSP toxins inhibit protein phosphatase and act upon
specific enzyme subunits, affecting regulatory processes, including
metabolism, membrane transport, secretion and cell division.
Various other HA toxins have not been chemically characterized.
Certain HA toxins appear to more strongly affect vertebrates such
as fish, birds, marine mammals and humans than invertebrates
Please cite this article in press as: Turner, J.T., Planktonic marine copepods and harmful algae. Harmful Algae (2014), http://dx.doi.org/
10.1016/j.hal.2013.12.001
such as crustaceans and bivalves (Robineau et al., 1991). This may
be due to decentralization of invertebrate nervous systems
compared to those of vertebrates.
It is often assumed that HA toxins are grazing deterrents to
discourage zooplankton grazers from eating HA. Indeed, there is
considerable laboratory evidence that some HA either are not
eaten by copepods and other zooplankters, or that after ingesting
HA, some grazers suffer adverse effects (reviewed by Turner, 2006).
However, toxic HA are consumed by various grazers during natural
blooms (reviewed by Turner, 2010), and various HA toxins become
concentrated in, and vectored through zooplankton and pelagic
food webs (reviewed by Doucette et al., 2005; Deeds et al., 2014;
Petitpas et al., 2014; Turner et al., 2000, 2005).
Toxicity of HA may be coincidental as HA toxins have been
suggested to be involved in functions in phytoplankton cells other
than deterrence of zooplankton grazers. Such suggested functions
include nitrogen storage, bioluminescence, chromosome structur-
al organization, pheromones for induction of sexuality, or toxins
may be vestigial remnants of archaic pathways for nucleic acid
biosynthesis (Cembella, 2003).
There is considerable variation in toxin potency, composition
and concentration between different clones or blooms of the same
HA species (Turner et al., 1998a; Waggett et al., 2012). Cellular
toxin levels can vary within a single clone with culture growth
phase (Taroncher-Oldenburg et al., 1997), turbulence (Juhl et al.,
2001), salinity (Grzebyk et al., 2003) or nutrient conditions (John
and Flynn, 2002; Leong et al., 2004; Hardison et al., 2012; Turner
et al., 1998a, and references therein). There can also be variability
in toxin content between different strains of the same algal species
grown under identical culture conditions (Etheridge and Roesler,
2005; Loret et al., 2002). Brevetoxins in the dinoflagellate Karenia
brevis may increase with osmotic stress caused by decreasing
salinity, as when cells move from oceanic to inshore waters (Errera
and Campbell, 2011), although this conclusion is not without
controversy (Sunda et al., 2013; Errera and Campbell, 2013).
4. HA toxins as copepod grazer deterrents
If HA toxins serve primarily as zooplankton grazing deterrents,
then grazers should selectively avoid feeding upon HA. However,
numerous species of copepods have been shown to feed upon
various toxic HA taxa. In many cases, there were no apparent
adverse effects from grazing on toxic algae (Table 1). However, in
many other cases, ingestion of toxic algae appeared to cause
adverse effects on copepods (Table 2). Adverse effects include
reduced feeding on HA taxa compared to control algae, reduced egg
production, reduced egg hatching success, reduced survival,
delayed development and/or behavioral changes. Much of this
variability likely relates to different concentrations of HA used as
food, different levels of toxins in food, and different tolerance for
various toxins by different copepod species from different
locations.
Most studies of copepod feeding interactions with toxic HA
have been laboratory experiments using unialgal cultures, often at
much higher concentrations than occur in natural blooms. Thus,
the relevance of such experiments to considerations of whether HA
toxins are grazing deterrents is questionable. Toxic HA taxa rarely
if ever bloom in nature in the absence of other non-toxic
phytoplankton, so results with unialgal cultures are usually not
representative of grazing during natural HA blooms. The fact that
HA are ingested by copepods in both laboratory experiments and
during natural blooms is evidenced by accumulation of HA toxins
in some copepods (Table 3). However, an important question is
whether HA toxins contribute to HA bloom development and
survival by deterring copepods and other zooplankton grazers
from grazing on a HA bloom?
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J.T. Turner / Harmful Algae xxx (2013) xxx–xxx 3

Table 1
Copepods that exhibit no apparent adverse effects from feeding upon HA.

Copepod HA species References

Acartia bifilosa Dinophysis norvegica + Dinophysis acuta Kozlowsky-Suzuki et al. (2006)

A. bifilosa Dinophysis spp. Setälä et al. (2009)
A. bifilosa Nodularia spumigena Gorokhova and Engström-Öst (2009), Koski et al. (2002)
Acartia clausi Pseudo-nitzschia multiseriesa Maneiro et al. (2005)
Acartia erythraea Chatonella antiqua Uye (1986)
Acartia hongi + Acartia omorii Pfiesteria piscicida Jeong et al. (2007)
Acartia hudsonica Alexandrium fundyenseb Colin and Dam (2002), Hassett (2003), Teegarden et al. (2001), Turner and
Anderson (1983), Turner and Borkman (2005), White (1981)
Acartia longiremis A. fundyense Turner and Borkman (2005)
A. omorii Heterosigma akashiwoc Uye and Takamatsu (1990)
Acartia pacifica C. antiqua Uye (1986)
Acartia tonsa A. fundyense Teegarden and Cembella (1996)
A. tonsa Karenia brevisd Turner and Tester (1989)
A. tonsa Karlodinium veneficume Saba et al. (2011)
A. tonsa P. piscicida Mallin et al. (1995), Roman et al. (2006)
A. tonsa P. multiseries Lincoln et al. (2001), Tester et al. (2001)
A. tonsa Prorocentrum minimum Saba et al. (2011)
A. tonsa Trichodesmium sp. (healthy intact cells) Guo and Tester (1994)
Calanus finmarchicus A. fundyense Hassett (2003), Teegarden et al. (2001, 2008), Turner and Borkman (2005)
C. finmarchicus P. multiseries Leandro et al. (2010b)
Calanus glacialis Pseudo-nitzschia seriata Tammilehto et al. (2012)
C. glacialis P. multiseries Windust (1992)
Calanus helgolandicus D. norvegica Jansen et al. (2006), Wexels Riser et al. (2003)
Calanus pacificus H. akashiwo Sykes and Huntley (1987)
Calanus sinicus Alexandrium tamarense Liu and Wang (2002)
C. sinicus C. antiqua Uye (1986)
Centropages typicus A. fundyense Turner and Borkman (2005)
C. typicus D. norvegica + D. acuta Kozlowsky-Suzuki et al. (2006)
Centropages yamadi C. antiqua Uye (1986)
Eurytemora affinis Dinophysis spp. Setälä et al. (2009)
E. affinis N. spumigena Gorokhova and Engström-Öst (2009), Koski et al. (2002)
Eurytemora herdmani A. fundyense Teegarden (1999), Teegarden and Cembella (1996)
Euterpina acutifrons K. veneficum Costa and Fernández (2002), Costa et al. (2005)
Labidocera aestiva K. brevis Turner and Tester (1989)
Oncaea venusta K. brevis Turner and Tester (1989)
Paracalanus parvus C. antiqua Uye (1986)
Pseudocalanus spp. A. fundyense Hassett (2003)
Pseudodiaptomus marinus C. antiqua Uye (1986)
P. marinus Chatonella marina Uye and Takamatsu (1990)
P. marinus Fibrocapsa japonica Uye and Takamatsu (1990)
P. marinus H. akashiwo Uye and Takamatsu (1990)
Temora longicornis D. norvegica + D. acuta Kozlowsky-Suzuki et al. (2006)
T. longicornis Dinophysis spp. Maneiro et al. (2002)
T. longicornis Phaeocystis globosa Koski et al. (2005)
T. longicornis P. multiseries Lincoln et al. (2001)
a
Previously known as Nitzschia pungens f. multiseries.
b
Previously known as Alexandrium tamarense, A. excavatum, Gonyaulax tamarensis, and Protogonyaulax tamarensis.
c
Previously known as Olisthodiscus luteus and Heterosigma carterae.
d
Previously known as Gymnodinium brevis, Gymnodinium breve, and Ptychodiscus brevis.
e
Previously known as Gyrodinium corsicum, Karlodinium micrum, and in some studies, K. armiger.

If copepods selectively avoid grazing on HA in nature, then
several possible mechanisms may be involved. These include
‘‘behavioral rejection’’ of HA before ingestion, or ‘‘physiological
incapacitation’’ of copepods after ingestion of HA, causing the
copepods to cease feeding (Ives, 1985, 1987). Although there is
evidence for both types of behavior (references in Turner and
Tester, 1997; Turner et al., 1998a), there is also evidence that many
copepods feed non-selectively upon toxic HA as well as other
phytoplankton and microzooplankton during HA blooms (refer-
ences in Turner, 2006). Since HA taxa usually comprise a small
fraction of the total assemblage of natural phytoplankton, even
during toxic HA blooms, non-selective grazing upon HA taxa may
not result in grazers ingesting enough HA toxins to cause effects,
particularly if most of the ingested food is other non-toxic
phytoplankton and microplankton.
Selective feeding means disproportionate ingestion of a given
food item. Thus, to properly evaluate ‘‘selective’’ versus ‘‘non-
selective’’ feeding requires quantification of the relative propor-
tions of different food items in the food that is ingested, compared
to the relative proportions of the same food items in the food
assemblage available to be eaten (see Turner and Anderson, 1983;
Turner and Borkman, 2005; Turner et al., 1998b). If a HA species
comprises a large proportion of the items in the available food
assemblage, but a small proportion of the food items actually
ingested from the available food assemblage, then that is evidence
of selection ‘‘against’’ the HA species. Conversely, if a HA species
comprises a greater proportion of the ingested food than of the
available food items, then that is evidence of selection ‘‘for’’ the HA
species. However, if the proportions of the HA species in the
ingested and available food assemblages are not significantly
different, then, by definition, that is ‘‘non-selective’’ feeding on the
HA species. Thus, selection is not just a function of behavior by the
grazers, but also of the abundance and composition of toxic and
non-toxic taxa in the natural food assemblage. In order to properly
evaluate selective or non-selective grazing of copepods on HA taxa,
one must examine grazing on all individual phytoplankton taxa in
a natural plankton assemblage with added copepods, compared
to initial and control replicates without added copepods, and

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Table 2
Copepods that exhibit apparent adverse effects (no or low feeding, low egg production, egg hatching success and/or survival, lethargy, incapacitation) from feeding upon HA.

Copepod HA species References

Acartia bifilosa Alexandrium ostenfeldii Sopanen et al. (2011)

A. bifilosa Aphanizomenon flos-aquae Sellner et al. (1994, 1996)
A. bifilosa Microcystis aeruginosa Balode and Strake (2004)
A. bifilosa Nodularia spumigena Balode and Strake (2004), Engström et al. (2000), Kozlowsky-Suzuki et al. (2003),
Lundgren et al. (2012), Sellner et al. (1994, 1996)
A. bifilosa Prymnesium parvuma Sopanen et al. (2006)
Acartia clausi Alexandrium lusitanicum Dutz (1998)
A. clausi Alexandrium minutum Barreiro et al. (2006), Barreiro et al. (2007), Frangópulos et al. (2000), Guisande et al. (2002b)
A. clausi Alexandrium tamarense Wohlrab et al. (2010)
A. clausi Dinophysis acuminata Carlsson et al. (1995), Maneiro et al. (2000)
A. clausi P. parvum Nejstgaard and Solberg (1996)
Acartia grani A. minutum Costa and Fernández (2002)
A. grani Gymnodinium catenatum Costa et al. (2012)
A. grani Karlodinium veneficumb Costa and Fernández (2002), Costa et al. (2005), Delgado and Alcaraz (1999)
Acartia hongi + Acartia omorii Amphidinium carterae Jeong et al. (2001)
Acartia hudsonica Alexandrium fundyensec Avery and Dam (2007), Avery et al. (2008), Colin and Dam (2002, 2003, 2007),
Ives (1985, 1987), Senft et al. (2011), Teegarden et al. (2008), Zheng et al. (2011)
A. hudsonica Heterosigma akashiwod Tomas and Deason (1981)
Acartia lilljeborgii (nauplii) Alexandrium tamiyavanichii Silva et al. (2013)
A. lilljeborgii (nauplii) Gonyaulax sp. Silva et al. (2013)
Acartia margalefi K. veneficum Vaqué et al. (2006)
A. omorii Karenia mikimotoie Uye and Takamatsu (1990)
Acartia tonsa A. fundyense Teegarden (1999)
A. tonsa A. minutum Selander et al. (2006)
A. tonsa Aureococcus anophagefferens Durbin and Durbin (1989), Lonsdale et al. (1996)
A. tonsa Aureoumbra lagunensis Buskey and Hyatt (1995), Buskey and Stockwell (1993)
A. tonsa Cochlodinium polykrikoides Jiang et al. (2009, 2010a, 2011)
A. tonsa Gymnodinium sanguineum Turner et al. (1998a)
A. tonsa H. akashiwo Tomas and Deason (1981)
A. tonsa Karenia brevisf Breier and Buskey (2007), Cohen et al. (2007), Collumb and Buskey (2004), Hong et al. (2012),
Prince et al. (2006), Speekmann et al. (2006), Turner et al. (1998a), Waggett et al. (2012)
A. tonsa Karlodinium armiger Berge et al. (2012)
A. tonsa K. veneficum Hong et al. (2012), Waggett et al. (2008)
A. tonsa N. spumigena Schmidt and Jónasdóttir (1997)
A. tonsa Phaeocystis globosa Tang et al. (2001)
A. tonsa Trichodesmium sp. (aged cultures) Guo and Tester (1994)
A. tonsa (nauplii) A. anophagefferens Smith et al. (2008)
Calanopia thompsoni Chatonella antiqua Uye (1986)
Calanus finmarchicus A. fundyense Turriff et al. (1995)
C. finmarchicus Pseudo-nitzschia seriata Tammilehto et al. (2012)
Calanus helgolandicus A. tamarense Wohlrab et al. (2010)
C. helgolandicus K. brevis Lauritano et al. (2013), Turner et al. (2012)
C. helgolandicus K. mikimotoi Gill and Harris (1987)
C. helgolandicus P. globosa Turner et al. (2002)
Calanus hyperboreus P. seriata Tammilehto et al. (2012)
Calanus pacificus K. brevis Huntley et al. (1986)
C. pacificus Protoceratium reticulatumg Huntley et al. (1986)
C. pacificus Scrippsiella trochoidea Huntley et al. (1986)
Centropages hamatus A. fundyense Teegarden (1999), Teegarden et al. (2008)
Centropages typicus D. acuminata Carlsson et al. (1995)
C. typicus K. brevis Cohen et al. (2007)
Eucalanus pileatus P. globosa Long and Hay (2006)
Eurytemora affinis A. ostenfeldii Sopanen et al. (2011)
E. affinis A. flos-aquae Sellner et al. (1994, 1996)
E. affinis M. aeruginosa Balode and Strake (2004)
E. affinis Nodularia sp. Koski et al. (1999a)
E. affinis N. spumigena Balode and Strake (2004), Engström et al. (2000), Kozlowsky-Suzuki et al. (2003),
Sellner et al. (1994, 1996)
E. affinis P. parvum Koski et al. (1999b), Sopanen et al. (2006, 2008)
Eurytemora herdmani A. fundyense Teegarden et al. (2008)
Euterpina acutifrons A. minutum Bagøien et al. (1996)
E. acutifrons D. acuminata Maneiro et al. (2000)
E. acutifrons G. catenatum Costa et al. (2012)
Isias clavipes D. acuminata Carlsson et al. (1995)
Labidocera rotundata C. antiqua Uye (1986)
Longipedia sp. (nauplii) Prorocentrum lima Silva et al. (2013)
Metridia lucens A. fundyense Hassett (2003)
Oithona similis A. tamarense Wohlrab et al. (2010)
Paracalanus sp. (nauplii) A. tamiyavanichii Silva et al. (2013)
Paracalanus sp. (nauplii) Gonyaulax sp. Silva et al. (2013)
Paracalanus parvus P. reticulatum Huntley et al. (1986)
Pseudocalanus sp. A. fundyense Ives (1985, 1987)
Pseudocalanus elongatus K. mikimotoi Schultz and Kiørboe (2009)
Pseudodiaptomus marinus H. akashiwo Uye and Takamatsu (1990)
P. marinus K. mikimotoi Uye and Takamatsu (1990)
Pseudodiaptomus pelagicus P. globosa Long and Hay (2006)

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Table 2 (Continued )

Copepod HA species References

Schmackeria inopinus H. akashiwo Yu et al. (2010)

Temora longicornis K. mikimotoi Gill and Harris (1987), Schultz and Kiørboe (2009)
T. longicornis P. globosa Dutz et al. (2005), Dutz and Koski (2006)
Temora stylifera P. globosa Turner et al. (2002)
Temora turbinata K. brevis Cohen et al. (2007)
Tortanus forcipatus C. antiqua Uye (1986)
a
Previously known as Prymnesium patelliferum.
b
Previously known as Gyrodinium corsicum, Karlodinium micrum, and in some studies, K. armiger.
c
Previously known as Alexandrium tamarense, A. excavatum, Gonyaulax tamarensis, and Protogonyaulax tamarensis.
d
Previously known as Olisthodiscus luteus and Heterosigma carterae.
e
Previously known as Gyrodinium aureolum and Gymnodinium nagasakiense.
f
Previously known as Gymnodinium brevis, Gymnodinium breve, and Ptychodiscus brevis.
g
Previously known as Gonyaulax grindleyi.

microscopically quantify all phytoplankton taxa, including the HA
taxa, by treating each initial, control, and experimental grazing
replicate as a quantitative phytoplankton sample.
Such experiments using natural plankton assemblages are
potentially complicated by cryptic trophic cascades within
experimental containers during experimental incubations (Calbet
and Saiz, 2013). Examples might include copepod predation upon
microzooplanktonic protists such as ciliates and heterotrophic
dinoflagellates, that are major consumers of some HA taxa. Thus,
the effects of such cascades might be that copepod predation on
microzooplankton protists would reduce microzooplankton pre-
dation upon HA phytoplankton. In one of the few experimental
evaluations of such cascades, Siuda and Dam (2010) found that
cascading indirect effects of copepod grazing on phytoplankton via
copepod removal of ciliates were minimal. Decreases in phyto-
plankton due to direct grazing by copepods was much greater than
any indirect increase in phytoplankton due to copepod predation
on ciliates, which reduced ciliate grazing on phytoplankton.
There have been a few investigations of copepod grazing on HA
taxa during natural HA blooms. Included have been studies during
blooms of Alexandrium spp. (Turner and Anderson, 1983;
Teegarden et al., 2001, 2008; Calbet et al., 2003; Campbell et al.,
2005; Turner and Borkman, 2005), Dinophysis spp. (Jansen et al.,
2006; Kozlowsky-Suzuki et al., 2006), and Karenia brevis (Turner
and Tester, 1989). In some cases, concentrations of HA taxa were
enhanced by inoculating natural plankton assemblages with
additional cultured HA cells (Turner and Anderson, 1983; Camp-
bell et al., 2005; Teegarden et al., 2008). With some variability, the

Table 3
Copepods shown to accumulate paralytic shellfish poisoning (PSP) toxins and other HA toxins from feeding upon HA.

Copepod HA species HA toxin References

Acartia bifilosa Dinophysis spp. Pectenotoxin Setälä et al. (2009)

A. bifilosa Nodularia spumigena Nodularin Kozlowsky-Suzuki et al. (2003)
Acartia hudsonica Alexandrium fundyensea PSP Dam and Haley (2011), Teegarden et al. (2003), White (1981)
A. hudsonica + others A. fundyense PSP Campbell et al. (2005)
Acartia clausi Alexandrium minutum PSP Barreiro et al. (2007), Guisande et al. (2002a,b)
A. clausi Alexandrium tamarense PSP Wohlrab et al. (2010)
A. clausi Pseudo-nitzschia multiseries Domoic acid Maneiro et al. (2005)
Acartia grani Gymnodinium catenatum PSP Costa et al. (2012)
Acartia omorii + others A. tamarense PSP Hamasaki et al. (2003)
Acartia tonsa A. fundyense PSP Teegarden and Cembella (1996)
A. tonsa Karenia brevisb Brevetoxins Cohen et al. (2007), Tester et al. (2000)
A. tonsa P. multiseries Domoic acid Lincoln et al. (2001), Tester et al. (2001)
Calanus finmarchicus A. fundyense PSP Durbin et al. (2002), Petitpas et al. (2014), Turriff et al. (1995)
C. finmarchicus P. multiseries Domoic acid Leandro et al. (2010b)
C. finmarchicus Pseudo-nitzschia seriata Domoic acid Tammilehto et al. (2012)
C. finmarchicus + others A. fundyense PSP Doucette et al. (2006)
Calanus glacialis P. seriata Domoic acid Tammilehto et al. (2012)
Calanus helgolandicus A. tamarense PSP Wohlrab et al. (2010)
Calanus hyperboreus P. seriata Domoic acid Tammilehto et al. (2012)
Centropages hamatus A. fundyense PSP Teegarden et al. (2003)
Centropages typicus Dinophysis norvegica + Dinophysis acuta Okadaic acid Kozlowsky-Suzuki et al. (2006)
C. typicus K. brevis Brevetoxins Cohen et al. (2007)
Eurytemora affinis Dinophysis spp. Pectenotoxin Setälä et al. (2009)
E. affinis N. spumigena Nodularin Karjalainen et al. (2006, 2008), Kozlowsky-Suzuki et al. (2003),
Lehtiniemi et al. (2002), Sopanen et al. (2009)
Eurytemora herdmani A. fundyense PSP Teegarden and Cembella (1996), Teegarden et al. (2003)
Euterpina acutifrons Gymnodinium catenatum PSP Costa et al. (2012)
Labidocera aestiva K. brevis Brevetoxins Tester et al. (2000)
Microsetella norvegica A. fundyense PSP Petitpas et al. (2014)
Oithona similis A. tamarense PSP Wohlrab et al. (2010)
Pseudocalanus spp. A. fundyense PSP Petitpas et al. (2014)
Temora longicornis P. multiseries Domoic acid Lincoln et al. (2001)
Temora turbinata K. brevis Brevetoxins Cohen et al. (2007), Tester et al. (2000)
Tigriopus californicus Alexandrium catenellac PSP Boyer et al. (1985)
a
Previously known as Alexandrium tamarense, A. excavatum, Gonyaulax tamarensis, and Protogonyaulax tamarensis.
b
Previously known as Gymnodinium brevis, Gymnodinium breve, and Ptychodiscus brevis.
c
Previously known as Gonyaulax catenella and Protogonyaulax catenella.

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emerging pattern from studies during natural blooms appears to
be that most copepods non-selectively graze toxic HA taxa in
proportion to their abundance, along with concurrent non-
selective grazing on other non-toxic phytoplankton taxa. General-
ly, the HA taxa comprised a minor component of the total
phytoplankton abundance during these blooms, except for the
1987 North Carolina red tide of K. brevis (Turner and Tester, 1989).
However, even at extremely low concentrations during natural HA
blooms, ingestion of HA by copepods has been detected using
molecular methods (Haley et al., 2011).
5. Induction of HA grazer deterrents by exposure to copepods
There are indications that exposure of certain HA taxa to
copepods induces increased HA toxin levels or other grazing
deterrents. Such deterrents may include increased cellular toxicity
levels, changes in dinoflagellate chain lengths or swimming
speeds, or changes in colony size in gelatinous phytoplankters
of the genus Phaeocystis.
Some dinoflagellates increase cellular toxicity in the presence of
copepods. Selander et al. (2006) found that waterborne cues from
the copepod Acartia tonsa induced increased PSP toxin production
in the dinoflagellate Alexandrium minutum. Induced A. minutum
contained significantly higher cellular toxin levels than controls,
and were grazed by copepods at lower rates than controls.
Ingestion of non-toxic alternative food (the dinoflagellate Pro-
rocentrum micans, which is similar in size and motility to A.
minutum) was unaffected by the presence of induced A. minutum.
Selander et al. (2006) concluded that the ability of A. minutum to
increase toxin production in response to the presence of copepod
grazers, and resulting resistance to grazing may facilitate HA
bloom formation and survival. Selander et al. (2008) found that
copepod-induced increases in PSP toxins were significantly higher
in high-nitrate conditions than in low-nitrate conditions, but
effects of phosphate were less consistent. Bergkvist et al. (2008)
found that copepod induction of increased PSP cellular toxin levels
in A. minutum was specific to the copepods involved. Two strains of
A. minutum responded to the presence of two copepod species
(Acartia clausi and Centropages typicus) with increased toxin levels,
but neither strain of A. minutum responded similarly to the
presence of the copepod Pseudocalanus sp. Bergkvist et al. (2008)
concluded that grazer-induced increases in PSP toxin levels were
grazer-specific responses, and that the potential ecological
importance of such responses was dependent on the composition
of the grazer community. Wohlrab et al. (2010) showed differences
in increased cellular toxin levels and altered gene expression
patterns in the dinoflagellate Alexandrium tamarense upon expo-
sure to waterborne chemical cues from three species of copepods
(Acartia clausi, Calanus helgolandicus, and Oithona similis). Wohlrab
et al. (2010) concluded that these responses resulted from co-
evolutionary processes, further suggesting that HA toxins are
grazer deterrents.
Presence of copepods has also been linked to induced grazer
defenses through changes in dinoflagellate chain lengths and
swimming speeds. Jiang et al. (2010b) found that natural
populations of the HA dinoflagellate Cochlodinium polykrikoides
from estuaries of Long Island, New York (USA) had longer chains
than laboratory cultures without copepods. Chain lengths of
natural populations were positively correlated with abundance of
the copepod Acartia tonsa. Chain length of C. polykrikoides
significantly increased when exposed to live copepods, or their
fresh exudates, suggesting that dissolved chemical cues released
by A. tonsa induced chain formation. Ingestion rates of four-cell
chains of C. polykrikoides were lower than those on single cells,
suggesting that chain formation might be a grazer defense by
increasing the proportions of large particles (42–52 mm chains) of
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the dinoflagellate that were larger than the optimal size (14 mm)
for the copepods to ingest. Chain formation may also increase the
swimming speed of C. polykrikoides chains, thereby making the
dinoflagellate chains harder for the copepods to catch than single
cells. Conversely, Selander et al. (2011) found that chain formation
in the dinoflagellate A. tamarense was strongly impaired by
waterborne cues from the copepod C. typicus, and that this resulted
in slower dinoflagellate swimming velocities, and lower encounter
rates with copepods, thereby reduced grazing rates. Selander et al.
(2011) concluded that dinoflagellates can regulate the balance
between predator avoidance and swimming speed by adjusting
chain length.
Selander et al. (2012) found that three copepods (Calanus sp.,
Centropages typicus, Acartia tonsa) simultaneously induced in-
creased toxicity and suppressed chain formation in Alexandrium
tamarense. Thus, the dinoflagellate became more toxic, and by
reducing chain lengths, reduced encounter rates with grazers, in
the presence of copepods. Copepods were caged and not in direct
contact with the dinoflagellates during these experiments,
indicating that the modifications in dinoflagellate toxicity and
chain length were induced by waterborne cues from the caged
copepods, and not the result of physical damage due to grazing.
The presence of grazers can also influence shifts in the size of
particles of colonial algae of the genus Phaeocystis. Species of
Phaeocystis can occur as both small single cells (4–6 mm) and large
gelatinous colonies of up to 30,000 mm in diameter (Long et al.,
2007). Single cells are grazed by microzooplankton such as ciliates
but not by most copepods, whereas colonies are eaten by some
copepods, but not most microzooplankton. Long et al. (2007) found
that chemical cues from ciliates of the genus Euplotes and the
copepod Acartia tonsa induced grazer-specific but opposite shifts in
size in Phaeocystis globosa. Chemical cues from copepods reduced
colony formation, which should act as a grazing deterrent, since
copepods fed more on colonies than single cells. Conversely,
chemical cues from ciliates enhanced colony formation, which
should also act as a grazing deterrent since ciliates grew faster when
feeding upon single cells than colonies of P. globosa. Similarly, Tang
et al. (2008) found that chemicals from the presence of natural
grazers from the Antarctic (dominated by the small copepods
Oithona similis, Microcalanus pygmaues, and Oncaea curvata) induced
increases in colony size in Phaeocystis antarctica, suggesting an
induced grazing deterrent through increased colony size.
6. Biogeographic aspects of copepod interactions with HA
toxins
There may be biogeographic aspects to interactions between
toxic HA and their copepod grazers. Copepods that co-occur with
HA taxa may have evolved tolerance to HA toxins, compared to
copepods from locations that do not routinely experience HA
blooms. Conversely, copepods that do not have co-evolutionary
experience with HA blooms may be more susceptible to impacts
from HA toxins.
There is both field and laboratory evidence in support of such a
biogeographic scenario. During the expatriate red tide of the Gulf
of Mexico HA dinoflagellate Karenia brevis that was carried to
North Carolina by the Gulf Stream in 1987, Turner and Tester
(1989) found that four species of copepods that grazed upon K.
brevis off North Carolina were species that routinely co-occurred
with K. brevis in the Gulf of Mexico. However, one species of
copepod, Centropages typicus, whose home range was coastal
waters off the northeastern United States, was atypically present
off North Carolina during the K. brevis bloom, and did not graze
upon K. brevis during this bloom. Conversely, C. typicus did graze on
other non-toxic HA species during the North Carolina K. brevis
bloom. Turner and Tester (1989) speculated that because K. brevis
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and C. typicus do not normally co-occur, that this copepod had no
co-evolutionary experience with feeding upon, or counteracting
the toxins of this dinoflagellate.
In a subsequent series of laboratory investigations (reviewed by
Dam, 2013), Colin and Dam (2002, 2003, 2004, 2007), Avery and
Dam (2007), Avery et al. (2008), and Zheng et al. (2011) showed
that populations of the copepod Acartia hudsonica from the Gulf of
Maine that had been historically exposed to the HA dinoflagellate
Alexandrium fundyense had higher rates of grazing, egg production,
egg hatching, growth, size at maturity, survival, toxin ingestion
rates (Dam and Haley, 2011) and tolerance to PSP toxins (Senft
et al., 2011) than copepods from Long Island Sound or New Jersey
that had little or no historical exposure to A. fundyense toxins. The
conclusion from these studies is that copepod populations with
longer history of exposure to HA toxins are more tolerant of HA
toxins than naı̈ve populations of copepods with little or no
exposure history (Dam, 2013).
Studies with other species also suggest biogeographic influ-
ences on the evolution of resistance to HA toxins by copepods.
Jiang et al. (2011) found that populations of the copepod Acartia
tonsa collected from Long Island (New York) bays during blooms of
the toxic dinoflagellate Cochlodinium polykrikoides were signifi-
cantly more resistant to the dinoflagellate than conspecific
copepods from nearby non-bloom estuaries. Using copepod egg
production rates as an indicator, Jiang et al. (2011) found that
resistance of a naı̈ve population of A. tonsa significantly increased
upon chronic exposure to C. polykrikoides over four copepod
generations. However, resistance was lost after a two-generation
relaxation of exposure of the copepods to the dinoflagellate. Jiang
et al. (2011) concluded that such rapid gain and loss of resistance
suggested that copepod adaptation to HA may result from
selection of resistant genotypes during ongoing blooms rather
than from exposure to previous blooms.
Diatoms are not typically considered to be HA taxa, with the
exception of species of the domoic-acid-producing genus Pseudo-
nitzschia. However, some diatoms produce polyunsaturated
aldehydes (PUAs) and other oxylipins that reduce egg production
and egg hatching success, and disrupt the development of offspring
of female copepods that eat these diatoms (reviewed by Ianora and
Miralto, 2010; Ianora et al., 2003). Such antiproliferative com-
pounds may sabotage future generations of copepods, allowing
diatom blooms to persist when they might have otherwise
declined due to copepod grazing pressure. Lauritano et al.
(2012) examined expression of stress-response genes for three
populations (Swedish west coast-North Sea, English Channel-
Atlantic and northern Adriatic Sea-Mediterranean) of the copepod
Calanus helgolandicus feeding on diets of the toxic-oxylipin-
producing diatom Skeletonema marinoi. In these three locations,
C. helgolandicus populations coexist with S. marinoi, but patterns of
exposure are different. On the west coast of Sweden, S. marinoi
differentiates into local populations and is the most abundant
diatom species, reaching maximum abundances twice a year. In
the English Channel this diatom is common but never the most
abundant diatom. In the northern Adriatic Sea, S. marinoi is the
most abundant diatom during the winter-spring bloom. PUAs have
been detected in all three S. marinoi populations. The three
copepod populations responded differently to the toxic S. marinoi
diet. The Swedish population of copepods was best at activating
stress/detoxification genes. The English Channel population of
copepods activated some of these genes, but the Adriatic
population was unable to activate any such genes, thereby making
the Adriatic copepods most susceptible to the toxic diatom diet.
These gene expression patterns agree with previous observations,
of strong reductions in copepod egg production and hatching
success for Adriatic C. helgolandicus feeding on S. marinoi in
laboratory cultures, or in natural blooms of S. marinoi in the
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7
northern Adriatic. Conversely, reductions in egg production and
hatching success were not as severe in English Channel and North
Sea C. helgolandicus.
Lauritano et al. (2012) concluded that there are genetic
population-level variations in mechanisms by which copepods
detoxify toxic diatoms, and that these variations may explain why
ingestion of diatoms sometimes did not cause reductions in
copepod egg production and egg hatching in some previous
studies. Such population-specific variations suggest that some
copepods have evolved tolerance to some phytoplankton toxins,
particularly in locations where copepods have had longer exposure
to these toxins.
Not all investigations of biogeographic aspects of copepod
interactions with HA taxa have produced results as clear-cut as the
aforementioned studies. Turner et al. (2012) examined feeding, egg
production, egg hatching success and survival of a copepod feeding
on a potentially-toxic dinoflagellate species with which it never
naturally co-occurs: the copepod Calanus helgolandicus from the
Mediterranean and the dinoflagellate Karenia brevis from the Gulf
of Mexico. Interactions of these two allopatric plankters were
compared with various co-occurring sympatric ones, including the
copepod Temora stylifera and a non-neurotoxic strain of the
dinoflagellate Alexandrium tamarense, both from the Mediterra-
nean off Naples, Italy, and the non-toxic dinoflagellate Prorocen-
trum minimum. Both Mediterranean copepods fed, reproduced and
survived on diets of K. brevis from the Gulf of Mexico, but not as
well as on diets of A. tamarense or P. minimum. Egg hatching success
of both copepods feeding on K. brevis declined sharply over five to
seven days of the experiments. The K. brevis strain was
subsequently shown not to contain any brevetoxins, but it
apparently contained other harmful metabolites. Also, the
Mediterranean copepod T. stylifera was adversely affected by
feeding on diets of the Mediterranean dinoflagellate A. tamarense.
Further, T. stylifera, which also occurs in the Gulf of Mexico, was far
more adversely affected by feeding on K. brevis than was C.
helgolandicus which never naturally co-occurs with K. brevis. Thus,
any putative biogeographic effects of copepods feeding on
allopatric versus sympatric dinoflagellates did not clearly emerge
from these experiments. However, both K. brevis and A. tamarense
apparently contained other compounds which may relate to the
recorded adverse effects on copepods.
Subsequently, Lauritano et al. (2013) examined expression of
stress genes in Calanus helgolandicus feeding on the same Karenia
brevis strain used in the studies of Turner et al. (2012). Expression
of stress-response genes when feeding on K. brevis indicated that C.
helgolandicus were under stress, and could not detoxify com-
pounds in the K. brevis diet, just as in the previous study of
Lauritano et al. (2012) for Mediterranean C. helgolandicus feeding
on a toxic diatom. Thus, the study of Lauritano et al. (2013)
supports previous studies which indicate that responses of
copepods to toxins or other chemicals in their diets have a genetic
basis which may exhibit biogeographic variation.
7. Impact of copepod grazing on HA bloom development and
termination
Zooplankton community grazing impacts on HA bloom
development and termination have been reviewed by Turner
and Tester (1997), Turner et al. (1998a), Turner (2006, 2010). In
some cases, grazing cannot prevent initiation and development of
HA blooms, but may contribute to bloom termination. Conversely,
grazing may inhibit initial bloom development, but once the bloom
is established, grazing cannot terminate a bloom. In most cases, the
grazing impact of microzooplankton such as ciliates and hetero-
trophic dinoflagellates vastly exceeds that of mesozooplankton
such as copepods (reviewed by Turner, 2006, 2010). Instances in
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which mesozoplankton grazing impact becomes potentially
important in bloom termination are usually associated with
seasonal high abundance of grazers such as polychaete larvae
(Turner and Anderson, 1983; Watras et al., 1985) or copepods
(Campbell et al., 2005). Conversely, low mesozooplankton
abundance and/or grazing pressure may have been factors
allowing development of the 1976 bloom of Ceratium tripos in
the New York Bight (Falkowski et al., 1980) and ‘‘brown tide’’
blooms in Narragansett Bay (Smayda and Villareal, 1989) and the
Laguna Madre of Texas (Buskey, 2008; Buskey and Stockwell,
1993; Buskey et al., 1997, 2001). Thus, as concluded by Teegarden
et al. (2008), grazer abundance may be the critical determinant of
grazing impact, rather than abundance or toxicity of HA cells.
8. Copepods and vectorial intoxication of pelagic food webs
Copepods are often initial entry points for vectorial intoxication
of pelagic food webs with HA toxins. Copepods ingest HA taxa and
accumulate HA toxins (Table 3). Copepods are then consumed by
larval or small fish, and HA toxins are passed up the food chain to
higher consumers such as large fish, seabirds and marine mammals
(reviewed by Turner and Tester, 1997; Turner et al., 1998a; Tester
et al., 2000). Even though some copepods appear to be rather
inefficient in retaining ingested HA toxins (Guisande et al., 2002b;
Hamasaki et al., 2003; Kozlowsky-Suzuki et al., 2003; Lehtiniemi
et al., 2002; Spyrakos et al., 2013; Teegarden et al., 2003), the
accumulated PSP toxins (Doucette et al., 2006; Durbin et al., 2002)
and domoic acid (Leandro et al., 2010a) remaining in copepods can
still intoxicate North Atlantic right whales (Eubalaena glacialis) that
feed directly on large copepods (Calanus finmarchicus). Ingested
PSP toxins have even killed humpback whales (Megaptera
novaeangliae) that consumed Atlantic mackerel (Scomber scom-
brus) that had fed on C. finmarchicus (Geraci et al., 1989).
9. Variability in results of studies of copepod grazing on HA
taxa
Previous reviews have noted that interactions between HA and
their grazers are complex, variable, and situation-specific (Turner
and Tester, 1997; Turner et al., 1998a; Turner, 2006). Much of the
variability is due to different chemical toxins occurring at different
levels in various cultures and strains of the same or different HA
species, with toxins having different effects on various grazers.
Many copepods and other grazers suffer adverse effects from
feeding on toxic HA (Table 2), leading to what have been
characterized by Sunda et al. (2006) as ‘‘ecosystem disruptive
algal blooms.’’ However, many other copepods appear to be
unaffected by feeding on toxic HA (Table 1), at least over the
duration of experiments. What should be done to resolve many of
the contradictory results from experiments on grazer interactions
with HA? Suggestions are presented below.
Much of the variability resulting from studies of zooplankton
grazing on toxic HA taxa likely results from variability in levels of
HA toxins in experimental diets. In experiments on grazing and egg
production by the copepod Acartia tonsa feeding on three different
strains of the putatively-toxic dinoflagellate Karenia brevis,
Waggett et al. (2012) confirmed that toxin content varied both
among and within strains. Brevetoxin analyses were performed
using liquid chromatography-mass spectrometry on the date of
each experiment, and the three strains were found to vary from
being non-toxic to 3-fold and 6-fold levels of toxicity during the
experiments. Waggett et al. (2012) concluded that ‘‘It is imperative
that (copepod) grazing and (egg) production experiments involving
toxic phytoplankton also include concurrent toxin analysis since toxins
vary with culture condition, growth phase, nutrient availability, and
between strains. . .’’ and that ‘‘. . .care should be taken before
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10.1016/j.hal.2013.12.001
assumptions regarding an entire species (of alga) are made based
on results of experiments using a single strain under a single set of
culture conditions.’’
Adherence to this recommendation would likely reduce much
of the inconsistency in results from studies of zooplankton grazing
and reproductive success while feeding on cultures or natural
blooms of HA. For instance, in an attempt to examine possible
biogeographic aspects of copepod feeding on a HA dinoflagellate,
Turner et al. (2012) found reduced grazing, egg production and egg
hatching success, compared to controls, for Mediterranean
copepods feeding on a putatively-toxic strain of the Gulf of
Mexico dinoflagellate K. brevis. These results would have likely
been attributed to HA toxins in the dinoflagellate diet had not
subsequent toxin analyses revealed that this strain of K. brevis
contained no brevetoxins. However, these results also suggested
the presence of some other unidentified chemical contributing to
the reductions in feeding, fecundity and egg viability on this diet.
Turner et al. (2012) concluded that ‘‘. . .understanding the biogeog-
raphy, must await defining the biochemistry of such harmful
algae:grazer interactions.’’
Measurements of toxicity should be made daily in studies of
zooplankton:HA interactions not only in laboratory studies with
phytoplankton cultures, but also in studies during natural HA
blooms. In studies of natural blooms of the toxic dinoflagellate
Alexandrium fundyense in the Gulf of Maine and on Georges Bank,
there were variations in both the total toxin levels per cell (Petitpas
et al., 2014) as well as the relative proportions of different PSP
toxins (Deeds et al., 2014) between the coastal Gulf of Maine and
Georges Bank. Furthermore, genotypic analyses based on micro-
satellite marker data collected during blooms in 2005–2007
indicated that A. fundyense populations from Georges Bank were
genetically distinct from coastal populations sampled in the Gulf of
Maine and the Bay of Fundy (M. Richlen, personal communication).
If zooplankton grazing investigators do not have the expertise and
infrastructure to measure HA toxin levels during their grazing
experiments, then they should collaborate with chemists who do.
Studies of copepods grazing on unialgal cultures of HA, though
interesting, are usually unrealistic. Blooms of HA do not occur in
the absence of other phytoplankton species, and grazers during
such blooms do not feed only upon HA taxa. Thus, grazing on HA
taxa is likely affected by concurrent grazing on non-HA taxa. Also,
many of the adverse effects noted for grazers feeding on cultures
likely relate to experimental diets with HA cells at higher
concentrations than during natural blooms of the same species.
In most natural HA blooms, HA taxa comprise only a minor
component of the total phytoplankton assemblage.
The most-straightforward way to study copepod grazing
impact on, or selective feeding for or against HA is to do so during
natural blooms, using copepods collected from bloom waters
feeding upon natural assemblages of HA and the smorgasbord of
other co-occurring phytoplankton at natural concentrations.
Grazing should be determined by quantitative microscopic
analyses of disappearance of HA and all other phytoplankton cells
in experimental compared to initial and control food suspensions,
using the formulae of Frost (1972). Experimental incubations
should be at the same temperatures as ambient temperatures in
the HA bloom waters. Such experiments can be done in shipboard
(examples include Turner and Borkman, 2005; Turner et al., 2001b)
or coastal laboratory (examples include Turner and Anderson,
1983; Turner and Tester, 1989; Turner et al., 1998b) settings. As
noted by Turner and Borkman (2005), ‘‘. . .it is important to approach
studies of zooplankton grazing on phytoplankton from the perspective
of a phytoplankton ecologist, ensuring that proper methodology is
used to quantify changes in abundances of various phytoplankton
taxa, upon which estimates of zooplankton grazing and selection
depend.’’ If zooplankton grazing scientists do not have the expertise
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and/or infrastructure to count and identify phytoplankton from
natural HA bloom assemblages, then they should collaborate with
phytoplankton ecologists who do.
It is important to preserve phytoplankton samples with
preservatives such as Lugol’s solution or Utermöhl’s solution
(Guillard, 1973) that do not destroy the delicate athecate
phytoplankton cells, which disintegrate upon preservation with
formalin. Such small athecate cells usually dominate the abun-
dance of natural phytoplankton assemblages, and are the most-
heavily-grazed component of such assemblages, even during
natural blooms of other larger thecate HA taxa (Turner and
Borkman, 2005).
Failure to account for grazing upon such athecate taxa
compromises any other conclusions concerning selection for or
against HA taxa during natural blooms. Also, as noted by Turner
(2006) ‘‘Even if HA toxins potentially discourage grazers from
sustained ingestion of HA species, in natural mixed phytoplankton
assemblages, and at the low concentrations of HA algae typically found
in blooms, effects of HA toxins may be minimized or diluted to the
irrelevant by concurrent ingestion of non-toxic co-occurring prey by
non-selective omnivorous grazing.’’ Teegarden et al. (2008) con-
cluded that ‘‘For many grazers, the toxicity of Alexandrium cells may
render them less palatable and thus less likely to be actively
selected,. . .but toxicity will probably not induce the selective feeding
necessary to confer specific protection.’’ Examination of selective
versus non-selective grazing on HA taxa during blooms requires
accurate assessments of grazing on all phytoplankton taxa during
blooms.
The vast majority of copepod grazing studies, including those on
HA taxa, have been conducted for approximately 24 h. This is often
not long enough to assess effects of various HA taxa on various
grazers. If experiments to quantify parameters such as copepod
ingestion rates, egg production rates, egg hatching success, and
mortality are conducted over periods of several days or even weeks,
in which the same copepods are transferred daily into fresh food
suspensions, there is often considerable day-to-day variability in
responses to identical concentrations of the same food suspensions
(numerous studies referenced by Ianora and Miralto, 2010; Ianora
et al., 2003; Turner et al., 2001a, 2012). Responses in some
parameters, particularly egg hatching success, typically decline
over time if female copepods continue to ingest teratogenic
compounds that interfere with reproduction, such as diatom
aldehydes or dinoflagellate toxins, even when copepod survival
remains high. Thus, examinations of effects of HA algae on copepods
and other grazers should be performed over extended periods, to
ensure that adverse effects on grazers which are absent after only
24 h do not subsequently become apparent after several days.
The impacts of grazing on HA blooms by copepods and other
zooplankton are highly variable and situation-specific. Examina-
tions of grazing impact on natural HA blooms must include
assessments of grazer abundance. Ideally, this should include
assessments before, during, and after termination of HA blooms. In
the few cases where ongoing monitoring programs have allowed
such assessments, the importance of not only grazing rates, but
grazer population abundance became apparent. Breakdowns of
community grazing at various trophic levels may allow blooms
such as the Texas brown tide to capitalize upon unusual
hydrographic conditions, initiating blooms that develop and
sustain themselves for extended periods.
Almost all examinations of copepod interactions with HA have
focused on calanoid copepods (Tables 1–3). However, cyclopoid
copepods, particularly of the genus Oithona, are usually much more
abundant than calanoids (Gallienne and Robins, 2001), particularly
in the near-surface waters where most HA blooms occur. The
ubiquitously-abundant cyclopoid Oithona similis is known to feed
primarily on microzooplanktonic protists such as ciliates and
Please cite this article in press as: Turner, J.T., Planktonic marine copepods and harmful algae. Harmful Algae (2014), http://dx.doi.org/
10.1016/j.hal.2013.12.001
9
heterotrophic dinoflagellates (Nakamura and Turner, 1997; Lons-
dale et al., 2000; Granéli and Turner, 2002). Thus, grazing on toxic
dinoflagellates and other HA taxa by copepods of the genus Oithona
would be expected to be a large component of copepod grazing
impact on HA blooms, but we have almost no information on such
interactions.
The fact that many HA blooms occur in coastal waters of the
temperate zone in spring is probably not coincidental. Such spring
blooms often begin in shallow coastal waters that are well-mixed
and nutrient-replete, where the euphotic zone may extend to near-
bottom depths, allowing the phytoplankton to take advantage of
seasonally-increasing insolation. At the beginning of such early
spring blooms, water temperatures are typically still cold, and
seasonal zooplankton populations may be just beginning to
develop. Thus, low grazing rates due to cold temperatures, coupled
with low grazer population abundances may contribute more to
reduced grazing pressure than toxin-associated grazer deterrence,
thereby allowing bloom development. Conversely, the causes of
HA bloom declines in late spring or summer cannot usually
separate effects of abundant grazer populations, depleted nutri-
ents, senescent HA populations, and increasing temperatures.
Understanding the interactions of such varied factors in the
development and decline of HA blooms requires pre- to post-
bloom monitoring and experimentation.
Predation patterns within plankton populations may perpetu-
ate some HA blooms. Omnivorous copepods can prey heavily on
microzooplankton protists (Granéli and Turner, 2002), which
appear to be the primary grazers of most HA blooms (Calbet et al.,
2003; Irigoien et al., 2005; Turner, 2010). Also, additional unusual
twists in predation patterns exist. For example, the toxic
dinoflagellate Karlodinium armiger has been shown to swarm
upon, attack, kill and eat the copepod Acartia tonsa, thereby
reducing copepod grazing pressure and perpetuating blooms of
this dinoflagellate (Berge et al., 2012).
In conclusion, the importance of grazing on HA blooms by
copepods and other zooplankton becomes apparent by its absence.
Due to a plethora of interacting factors, development of a HA bloom
implies that HA taxa have outgrown or otherwise thwarted the
ability of zooplankton grazers to regulate the bloom. Thus,
zooplankton grazing ecology is an important aspect of HA bloom
ecology.
Acknowledgements
I thank anonymous reviewers for criticism, and Chrissy Petitpas
for extensive editing. This paper is ECOHAB contribution number
786.[SS]
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