Zooplankton grazing on Phaeocystis: a quantitative review ... · and future challenges ... et al....

Biogeochemistry (2007) 83:147–172
DOI 10.1007/s10533-007-9098-y
REVIEW

Zooplankton grazing on Phaeocystis: a quantitative review and future challenges

Jens C. Nejstgaard · Kam W. Tang · Michael Steinke · Jörg Dutz · Marja Koski · Elvire Antajan · Jeremy D. Long

Received: 23 May 2006 / Accepted: 16 November 2006 / Published online: 20 April 2007© Springer Science+Business Media B.V. 2007

Abstract The worldwide colony-forming hapto-phyte phytoplankton Phaeocystis spp. are key organ-isms in trophic and biogeochemical processes in theocean. Many organisms from protists to Wsh ingestcells and/or colonies of Phaeocystis. Reports on spe-ciWc mortality of Phaeocystis in natural plankton ormixed prey due to grazing by zooplankton, especiallyprotozooplankton, are still limited. Reported feedingrates vary widely for both crustaceans and protistsfeeding on even the same Phaeocystis types and sizes.Quantitative analysis of available data showed that:(1) laboratory-derived crustacean grazing rates onmonocultures of Phaeocystis may have been overesti-mated compared to feeding in natural planktoncommunities, and should be treated with caution;

(2) formation of colonies by P. globosa appeared toreduce predation by small copepods (e.g., Acartia,Pseudocalanus, Temora and Centropages), whereaslarge copepods (e.g., Calanus spp.) were able to feedon colonies of Phaeocystis pouchetii; (3) physiologi-cal diVerences between diVerent growth states, spe-cies, strains, cell types, and laboratory culture versusnatural assemblages may explain most of the varia-tions in reported feeding rates; (4) chemical signalingbetween predator and prey may be a major factor con-trolling grazing on Phaeocystis; (5) it is unclear towhat extent diVerent zooplankton, especially proto-zooplankton, feed on the diVerent life forms of Phae-ocystis in situ. To better understand the mechanismscontrolling zooplankton grazing in situ, future studies

J. C. Nejstgaard (&)UNIFOB AS, Department of Biology, University of Bergen, Bergen High Technology Centre, 5020 Bergen, Norwaye-mail: [email protected]

K. W. TangVirginia Institute of Marine Science, 1208 Greate Road, Gloucester Point, VA, 23062, USA

M. SteinkeDepartment of Biological Sciences, University of Essex, Wivenhoe Park, Colchester, CO4 3SQ, UK

J. DutzInstitute for Baltic Sea Research, Seestraße 15, 18119 Rostock Warnemunde, Germany

M. KoskiDanish Institute for Fisheries Research, Kavalergården 6, 2920 Charlottenlund, Denmark

E. AntajanLaboratoire d’Océanographie de Villefranche, Université Pierre et Marie Curie-Paris6, 06230 Villefranche-sur-Mer, France

E. AntajanLaboratoire d’Océanographie de Villefranche, CNRS, 06230 Villefranche-sur-Mer, France

J. D. LongNortheastern University Marine Science Center, 430 Nahant Road, Nahant, MA, 01908, USA

123

148 Biogeochemistry (2007) 83:147–172

should aim at quantifying speciWc feeding rates ondiVerent Phaeocystis species, strains, cell types, preysizes and growth states, and account for chemical sig-naling between the predator and prey. Recently devel-oped molecular tools are promising approaches toachieve this goal in the future.

Keywords Colony formation · DMS · Gut pigment · Molecular methods · Microzooplankton · Phaeocystis · antarctica · Predator defense

Introduction

The haptophyte Phaeocystis is a dominant phyto-plankton genus in tropical to polar seas (Baumannet al. 1994). They are key species in marine foodwebs and biogeochemical cycles, e.g., as major pro-ducers of carbon and climatically important sulWdecompounds (Liss et al. 1994; Alderkamp et al. thisvolume; Stefels et al. this volume). Three major spe-cies: P. globosa ScherVel, P. pouchetii (Hariot) Lag-erheim and P. antarctica Karsten (Medlin andZingone this volume) exist in two main morphotypes:small single cells and mucilaginous colonies (seeRousseau et al. this volume for details on the diVerentcell and morphotypes).

The success of Phaeocystis has been ascribed to anumber of factors, including escaping from grazingby its dramatic ability to shift morphotype betweensolitary Xagellates of a few micrometers to largemucous colonies up to several cm in diameter(Weisse et al. 1994; Chen et al. 2002; Schoemannet al. 2005; Veldhuis and Wassmann 2005; Rousseauet al. this volume). For a phytoplankton bloom toform, the sum of growth and accumulation must belarger than the sum of loss due to horizontal and verti-cal advection, sinking, lysis and predation (e.g.,Smayda 1997; Banse 1994). Advection is beyond thecontrol of all phytoplankton, and thus not likely to bea strong selective force for Phaeocystis (but see Seu-ront et al. this volume). Neither does the growth rateof Phaeocystis appear to be exceptionally high rela-tive to other bloom-forming phytoplankton, such asdiatoms (Hegarty and Villareal 1988). Indeed, inmany Weld and mesocosm studies Phaeocystis bloomsco-occurred with, or followed the demise of, diatomblooms (Peperzak et al. 1998; GoVart et al. 2000;Rousseau et al. 2002; Tungaraza et al. 2003; Larsen

et al. 2004). Sinking loss of Phaeocystis also seems tobe small for the large colonies (Reigstad and Wass-mann this volume). This could be partly due to theballoon-like characteristics of the colonies: colonialcells are embedded in a thin mucous skin whereas theinterior of the colonies is hollow (van Rijssel et al.1997). Although single cells are susceptible to virallysis, an intact mucous skin may protect colonialPhaeocystis cells from viral lysis and other infections(reviewed by Brussaard et al. this volume). A remain-ing possible explanation for the success of Phaeocys-tis despite its moderate growth rate is its ability toreduce grazing mortality, which is the focus of thisreview article.

Grazing on Phaeocystis (mainly P. globosa and P.pouchetii) has been studied since the beginning of thelast century (e.g., Lebour 1920, 1922), and a widerange of organisms have been reported to be able toingest Phaeocystis (Table 1). Unfortunately, most ofthe early studies were based on light microscopy ofgut contents of the grazers, and neither feeding ratenor detailed description of the prey species was avail-able (see Notes in Table 1, and further discussionbelow). It was not until the 1980s that direct quantita-tive studies on zooplankton feeding on Phaeocystiswere reported (reviewed in Peperzak 2002; Rousseauet al. 2000; Schoemann et al. 2005; Weisse et al.1994). Published grazing rates span wide ranges evenfor the same predators feeding on the same Phaeocys-tis species, morphotype and food concentration. Thisindicates that the widely accepted view of grazingvulnerability as a function of predator-to-prey sizeratio and prey abundance (Frost 1972; Hansen et al.1994a) for a given predator type (Hansen et al. 1997)may be compounded by other factors controllinggrazing on Phaeocystis.

Although copepods and other organisms may ingestPhaeocystis spp. (Table 1), at least when they are inpalatable condition (Estep et al. 1990; Long and Hay2006), there are also reports of reduced zooplanktonfeeding and abundance during blooms of Phaeocystis(Table 2) and low reproductive output in copepods,even when feeding rates are relatively high (Verityand Smayda 1989; Turner et al. 2002; Klein Bretelerand Koski 2003; Long and Hay 2006). Several authorshave previously reviewed various negative eVects ofPhaeocystis on diVerent organisms (e.g., Weisse et al.1994; Turner et al. 2002; Schoemann et al. 2005); andwe provide an updated summary in Table 2. However,

123

Biogeochemistry (2007) 83:147–172 149
T
able

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ang

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04)

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oid

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cel

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ies

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n ex

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men

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icro

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anse

n (1

992,

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5),

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and

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g (2

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arin

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ujar

din

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bosa

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le c

ells

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batio

n ex

peri

men

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n et

al. (

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iate

s

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lote

s sp

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anta

rcti

casi

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ies

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ently

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ield

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ith (

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ells

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onie

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rim

ents

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004)

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icos

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ella

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ulat

a (E

hren

berg

)–

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sing

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ells

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rosc

opy

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iraa

l and

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enek

amp

(198

6)

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man

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rmis

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gaar

d–

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le c

ells

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batio

n ex

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ang

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01)

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ahl)

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etz

& F

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asi

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cel

lsin

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tion

expe

rim

ents

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g et

al. (

2001

)

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mbi

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psis

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min

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auré

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mie

t–

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lobo

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cel

ls a

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ies

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batio

n ex

peri

men

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anse

n (1

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3)

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g et

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roid

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123

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able

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ntin

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zer

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geO

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ilus

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er c

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tri a

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ares

chi (

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)

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ovén

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epod

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n.)

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reen

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ains

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babl

y P

haeo

cyst

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man

y”in

situ

gut

mic

rosc

opy

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our

(192

2)

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rtia

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inhe

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fem

ale

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isi

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cel

ls a

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ies

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batio

n ex

peri

men

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mal

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tii

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sted

onl

y co

loni

es <

100

�m

incu

batio

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peri

men

tsH

anse

n et

al. (

1994

b)

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tons

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ana

CV

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mal

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obos

a, p

ouch

etii

sing

le c

ells

and

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onie

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tion

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rim

ents

Tan

g et

al. (

2001

), T

ang

and

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ó (2

003)

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ity (

2000

),

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ity

and

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da (

1989

)

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mal

ocer

a pa

tter

soni

T

empe

lton

cope

podi

tes

?sp

.“P

haeo

cyst

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insi

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ut m

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scop

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ebou

r (1

922)

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anoi

des

sp.

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epod

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arct

ica

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entl

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cel

lsgu

t mic

rosc

opy

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ang

unpu

blis

hed

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anus

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arch

icus

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unn.

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r (1

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anus

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isi

ngle

cel

ls a

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olon

ies

incu

batio

n ex

peri

men

tsH

anse

n et

al. (

1990

), T

ande

a

nd B

åmst

edt (

1987

)

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anus

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cial

is J

asch

nov

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uche

tii

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nies

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batio

n ex

peri

men

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step

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990)

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anus

hel

gola

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us (

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us)

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tes

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80 �

mcf

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bosa

sing

le c

ells

and

col

onie

sin

cuba

tion

expe

rim

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Han

sen

(199

2, 1

995)

, T

urne

r et

al. (

2002

)

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anus

hyp

erbo

reus

(K

røye

r)C

IV-C

VI

fem

ale

pouc

heti

isi

ngle

cel

ls a

nd c

olon

ies

incu

batio

n ex

peri

men

tsE

step

eta

l. (1

990)

, Hun

tley

etal

. (19

87),

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de a

nd

Båm

sted

t (19

87)

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trop

ages

ham

atus

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jebo

rgco

pepo

dite

s >

280

�m

cf. g

lobo

sasi

ngle

cel

ls a

nd c

olon

ies

incu

batio

n ex

peri

men

tsH

anse

n (1

995)

Cen

trop

ages

ham

atus

Lill

jebo

rgco

pepo

dite

s ?

cf. g

lobo

saco

loni

es?

“Pha

eocy

stis

blad

ders

”in

situ

gut

mic

rosc

opy

Jone

s an

d H

aq (

1963

)

Cen

trop

ages

typi

cus

Krø

yer

cope

podi

tes

?sp

.“s

pore

s”in

situ

gut

mic

rosc

opy

Leb

our

(192

2)

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alan

us p

ilea

tus

Gie

sbre

cht

CV

I fe

mal

egl

obos

asi

ngle

cel

ls a

nd c

olon

ies

incu

batio

n ex

peri

men

tsL

ong

and

Hay

(20

06)

Met

ridi

a ge

rlac

hi G

iesb

rech

tco

pepo

dite

s ?

pouc

heti

i (in

Ant

arct

ica)

colo

nies

0.0

5–1.

5m

min

cuba

tion

expe

rim

ents

Schn

ack

(198

3)

123

T
able

1co

ntin

ued

Gra

zer

Dev

elop

men

tal s

tage

Pha

eocy

stis

spe

cies

type

/sta

geO

berv

atio

n m

etho

dR

efer

ence

s

Mic

roca

lanu

s sp

.C

opep

odite

san

tarc

tica

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resc

ently

labe

led

sing

lece

llsgu

t mic

rosc

opy

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ang

unpu

blis

hed

Par

euch

aeta

ant

arct

ica

(Gie

sbre

cht)

cope

podi

tes

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uche

tii (

in A

ntar

ctic

a)co

loni

es 0

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1.5

mm

incu

bati

on e

xper

imen

tsSc

hnac

k (1

983)

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udoc

alan

us e

long

atus

(B

oeck

)co

pepo

dite

s >

280

�m

cf. g

lobo

sasi

ngle

cel

ls a

nd c

olon

ies

incu

bati

on e

xper

imen

tsH

anse

n (1

992,

199

5)

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agic

us

Her

rick

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mal

egl

obos

asi

ngle

cel

ls a

nd c

olon

ies

incu

bati

on e

xper

imen

tsL

ong

and

Hay

(20

06)

Tem

ora

long

icor

nis

Mül

ler

naup

lii t

o ad

ults

glob

osa

sing

le c

ells

and

col

onie

sin

cuba

tion

exp

erim

ents

Dut

z an

d K

oski

(20

06),

K

oski

eta

l. (2

005)

, H

anse

n (1

992,

199

5)

Tem

ora

long

icor

nis

Mül

ler

cope

podi

tes

?cf

. glo

bosa

colo

nies

? “P

haeo

cyst

isbl

adde

rs”

insi

tu g

ut m

icro

scop

yJo

nes

and

Haq

(19

63)

Tem

ora

long

icor

nis

Mül

ler

cope

podi

tes

?sp

.“g

reen

cel

ls, p

roba

bly

Pha

eocy

stis

”in

situ

gut

mic

rosc

opy

Leb

our

(192

2)

Tem

ora

styl

ifer

a D

ana

adul

t fem

ale

appe

ared

sim

ilar

to g

lobo

sacu

lture

d si

ngle

cel

ls a

nd

colo

nies

incu

bati

on e

xper

imen

tsT

urne

r et

al. (

2002

)

Cop

epod

s, c

yclo

poid

s

Cor

ycae

us a

ngli

cus

Lub

bock

cope

podi

tes

?sp

.“P

haeo

cyst

is in

sev

eral

”in

situ

gut

mic

rosc

opy

Leb

our

(192

2)

Oit

hona

nan

a G

iesb

rech

tco

pepo

dite

s ?

cf. g

lobo

saco

loni

es?

“Pha

eocy

stis

bl

adde

rs”

insi

tu g

ut m

icro

scop

yJo

nes

and

Haq

(19

63)

Oit

hona

sp.

cope

podi

tes

anta

rcti

caX

uore

scen

tly la

bele

d si

ngle

cel

lsgu

t mic

rosc

opy

K. T

ang

unpu

blis

hed

Onc

aea

curv

ata

(Gun

n.)

adul

t fem

ale

cf. p

ouch

etii

(in

Ant

arct

ica)

colo

nies

incu

bati

on e

xper

imen

tsM

etz

(199

8)

Cop

epod

s, h

arpa

ctic

oids

Eut

erpi

na a

cuti

fron

s (D

ana)

cope

podi

tes

?sp

.“X

agel

late

s...e

spec

ially

Pha

eocy

stis

”in

situ

gut

mic

rosc

opy

Leb

our

(192

2)

Cir

ripe

des

Bal

anus

cre

natu

s B

rugu

ière

naup

lii

cf. g

lobo

sasi

ngle

cel

ls a

nd c

olon

ies

incu

bati

on e

xper

imen

tsH

anse

n (1

992,

199

5)

“Cir

ripe

des”

naup

lii

sp.

“pro

babl

y P

haeo

cyst

is”

insi

tu g

ut m

icro

scop

yL

ebou

r (1

922)

Lon

gipe

da m

inor

T. &

A. S

cott

adul

t fem

ale

sp.

colo

nies

incu

bati

on, v

isua

l in

spec

tion

Nic

holls

(19

35)

Lon

gipe

da s

cott

i G.O

.Sar

sad

ult f

emal

esp

.co

loni

esin

cuba

tion

, vis

ual

insp

ecti

onN

icho

lls (

1935

)

123

T
able

1co

ntin

ued

(¡)

deno

tes

no i

nfor

mat

ion/

not

appl

icab

le.

(?)

deno

tes

likel

y bu

t un

clea

r. N

ote

that

spe

cies

com

posi

tion

wit

hin

the

genu

s P

haeo

cyst

is h

as b

een

deba

ted

(Bau

man

n et

al.

1994

;S

ourn

ia 1

988)

. Bec

ause

the

solit

ary

cell

s of

P. g

lobo

sa, P

. pou

chet

ii a

nd o

ther

s m

ay n

ot b

e di

stin

guis

habl

e by

ligh

t mic

rosc

opy,

rep

orts

bef

ore

1980

cou

ld b

e m

isle

adin

g [e

.g.,

the

spec

ies

in A

ntar

ctic

a re

port

ed b

y Sc

hnac

k (1

983)

and

Met

z (1

998)

may

like

ly b

e P

. ant

arct

ica,

rat

her

than

P. p

ouch

etii

]. W

here

mul

tiple

ref

eren

ces

are

avai

labl

e (m

ostl

y fo

r ca

l-an

oid

cope

pods

) on

ly s

elec

ted

repr

esen

tativ

e re

fere

nces

are

sho

wn

here

. See

text

for

mor

e re

fere

nces

.

Gra

zer

Dev

elop

men

tal s

tage

Pha

eocy

stis

spe

cies

type

/sta

geO

berv

atio

n m

etho

dR

efer

ence

s

Am

phip

ods

Pon

toge

neia

ant

arct

ica

Che

vreu

xha

tchi

ling

s (2

mm

)-ad

ults

anta

rcti

ca“g

reen

pla

stid

ic d

ebri

s...

prob

ably

indi

cate

inge

stio

nof

Pha

eocy

stis

ant

arct

ica”

insi

tu g

ut m

icro

scop

yR

icha

rdso

n an

d W

hita

ker

(197

9)

Eup

haus

iids

Eup

haus

ia s

uper

ba D

ana

sp.

insi

tu g

ut m

icro

scop

ySi

ebur

th (

1960

)

Eup

haus

ia s

uper

ba D

ana

35–4

5m

man

tarc

tica

sing

le c

ells

and

co

loni

es <

500

�min

cuba

tion

exp

erim

ents

Hab

erm

an e

tal.

(200

3)

Thy

sano

essa

iner

mis

(K

røye

r)ca

rapa

ce c

a 5

mm

po

uche

tii

inge

sted

onl

y co

loni

es >

20

�m

incu

bati

on e

xper

imen

tsH

anse

n et

al. (

1994

b)

Thy

sano

essa

ras

chii

(M

. Sar

s)ca

rapa

ce c

a 5

mm

po

uche

tii

inge

sted

onl

y co

loni

es >

20

�m

incu

bati

on e

xper

imen

tsH

anse

n et

al. (

1994

b)

Dec

apod

s

Cra

b (u

nide

ntiW

ed)

zoëa

sp.

“Pha

eocy

stis

”in

situ

gut

mic

rosc

opy

Leb

our

(192

2)

Gal

athe

a in

term

edia

Lill

jebo

rgm

egal

opa

cf. g

lobo

sasi

ngle

cel

ls a

nd c

olon

ies

incu

bati

on e

xper

imen

tsH

anse

n (1

992,

199

5)

Por

cell

ana

sp.

“lar

va”

sp.

“gre

en s

pore

s, p

roba

bly

Pha

eocy

stis

”in

situ

gut

mic

rosc

opy

Leb

our

(192

2)

Por

tunu

s de

pura

tor

(Lin

naeu

s)zo

ëa I

II-V

cf. g

lobo

sasi

ngle

cel

ls a

nd c

olon

ies

incu

bati

on e

xper

imen

tsH

anse

n (1

992,

199

5)

Por

tunu

s ho

lsat

us (

Fab

rici

us)

meg

alop

acf

. glo

bosa

sing

le c

ells

and

col

onie

sin

cuba

tion

exp

erim

ents

Han

sen

(199

2, 1

995)

App

endi

cula

rian

s

Meg

aloc

ercu

s hu

xley

i (R

itte

r)-

sp.

smal

l col

ony

insi

tu f

aeca

l pel

let

mic

rosc

opy

Gor

sky

etal

. (19

99)

Fis

h

Gad

us m

orhu

a L

.la

rvae

< 0

.2m

g/4

mm

pouc

heti

ico

loni

esin

situ

gut

mic

rosc

opy

Kro

gsta

d (1

989)

, L

øken

(19

90)

Ple

uron

ecte

s X

esus

L.

larv

ae <

11

mm

sp.

colo

nies

incu

bati

on, v

isua

l in

spec

tion

and

insi

tu

gut

mic

rosc

opy

Leb

our

(192

0)

Scom

ber

scom

brus

L.

larg

e fr

om W

sh

catc

hes

glob

osa

“ph

ytop

lank

ton

chieX

y P

. glo

bosa

” as

soci

ated

with

jelly

pro

babl

y co

loni

es

insi

tu g

ut m

icro

scop

yB

ulle

n (1

908)

123


some of these data were derived from ecologicallyunrealistic organisms or assays and should be inter-preted with caution (see discussion below). Further,positive correlations between Phaeocystis abundanceand mesozooplankton in the Weld have also beenreported, and some of the negative eVects have beendebated and ascribed to other organisms (see Notes inTable 2). Furthermore, results from fatty acid analysisindicate that dominating crustacean zooplankton mayderive a major part of their diet from P. pouchetii innorthern latitudes (Sargent et al. 1985) and fromP. globosa in lower latitudes (Hamm and Rousseau2003), suggesting that Phaeocystis do enter the foodweb.

A number of factors have been shown to controlpredation on this enigmatic genus: predator-to-preysize ratio, predator species and stage, prey species,morphotype, growth state and abundance (reviewedin Weisse et al. 1994; Rousseau et al. 2000; Peperzak2002; Schoemann et al. 2005). However, to ourknowledge, a quantitative analysis of the interactiveeVect of these factors has not been attempted. Usingavailable literature, we attempt to quantify the relativeimportance and interactions among some of these fac-tors in controlling zooplankton grazing on Phaeocys-tis spp. We also review recent Wndings on variousunique aspects of the life history and physiology ofPhaeocystis spp., and how they aVect zooplanktongrazing. Last, we discuss the need for new methodo-logical approaches to address some of the remainingquestions concerning zooplankton grazing on Phaeo-cystis.

Grazing on Phaeocystis: quantitative patterns in published data

Reports on copepods and other crustaceans dominateavailable zooplankton grazing data on Phaeocystisspp. These data show a wide range of rates, even forsimilar predator-prey combinations. We thereforeattempt to summarize available quantitative data inrelation to some of the mechanisms proposed to con-trol the feeding on Phaeocystis. The shortage of quan-titative feeding studies on microzooplankton andPhaeocystis was pointed out already a decade ago(Weisse et al. 1994), and the number of such studiesis still limited, especially for protozoan microzoo-plankton, whether using laboratory cultures (Table 3)

or natural plankton assemblages (Table 4) as food.Due to the shortage of protozooplankton data a gen-eral statistical analysis of the factors controlling theirgrazing on Phaeocystis cannot yet be performed, butthe available data will be discussed further below.

Crustacean zooplankton grazing on Phaeocystis: is there a general pattern?

It is generally assumed that a shift from single cell tocolony may be part of Phaeocystis defense againstgrazing by microzooplankton (Weisse et al. 1994;Rousseau et al. 2000; Peperzak 2002; Schoemannet al. 2005). Because of the ability of Phaeocystis tovary its functional prey size by forming colonies, it isoften considered as dual species (sensu Turner et al.2002): colonies can be referred to as macroplanktonand are assumed to be suitable food for zooplanktonand nekton, while the solitary nanoplankton areassumed to be vigorously grazed by microzooplank-ton (Lebour 1922; Hollowday 1949; Admiraal andVenekamp 1986; Weisse and ScheVel-Möser 1990).On the other hand an increase in size may result in amore suitable prey size range for larger predatorssuch as crustacean zooplankton. For palatable prey,ingestion rates generally increase from small prey tothe optimum prey size before the prey becomes toolarge to handle or ingest (Frost 1972; Hansen et al.1994a). Thus, size may be a major factor controllingpredation on Phaeocystis.

Many studies showed that the size of Phaeocystisstrongly inXuences the feeding rates of diVerentlysized metazoan predators. Hansen et al. (1990)reported that Calanus Wnmarchicus copepodites (CI-V) showed lower feeding rate on P. pouchetii colo-nies of >100 �m than similarly sized diatoms, whilein the 30–100 �m size range feeding rates on diatomsand colonies were similar. Tande and Båmstedt(1987) showed that copepodite stage V of C. Wnmar-chicus fed equally well on P. pouchetii single cellsand the diatom Chaetoceros furcellatus, whereasHuntley et al. (1987), using the larger copepodC. hyperboreus CIV-V, reported much higher grazingrates on colonies 25–200 �m and >200 �m than onsingle cells of P. pouchetii or the diatom Chaetocerossocialis. In a study with grazers of diVerent sizesfeeding on P. pouchetii, Hansen et al. (1994b)observed an optimal predator-to-prey size ratio forfeeding and an upper size ratio above which no ingestion

123


Table 2 Negative eVects on various organisms ascribed to Phaeocystis spp., with notes on contradictory reports

EVect Note References

Protists and other microbes

Defence against viral attacks by intact colony membranes Reviewed by Brussaard et al. (this volume)

Antibiotic to bacteria in the acid environment of penguin guts. A Sieburth (1960, 1961)

Haemolytic activity in laboratory, or correlated with abundance of P. pouchetii during blooms of natural planktonin mesocosms

Stabell et al. (1999), van Rijssel et al. (this volume)

Suggested allelopathy, e.g., possible negative intercations by P. pouchetii on T. nordenskioeldii and Skeletonema costatum in vitro. Rapid decrease in abundance of Thalassiosira nordenskioeldii and Ebria sp. during a bloom of P. pouchetii.

Barnard et al. (1984), Smayda (1973)

Allelopathy, Wltrates from mesocosm blooms of P. pouchetii and laboratory cultures of P. globosa resulting in reduced growth and lysis of the cryptophyte phytoplankton Rhodomonas baltica.

Long (Unpublished data)

Lack of feeding of the ciliates Mesodinium pulex and Strombidium elegans in laboratory experiments despite high concentrations of P. globosa and no alternative food.

Hansen et al. (1993), Tang et al. (2001)

Low biomass of bacteria and protozooplankton during blooms of colonial Phaeocystis

B van Boekel et al. (1992)

Metazooplankton

Many copepods show low abundances, development, gut content and/or much lower feeding activity compared to alternative food such as diatoms, during blooms of Phaeocystis

C Bautista et al. (1992), Breton et al. (1999), Daro (1985), Davies et al. (1992), Frangoulis et al. (2001), Gasparini et al. (2000), Hansen and van Boekel (1991), Turner (1994), Weisse et al. (1994)

Low feeding by Calanus spp. and Metridia longa on actively growing colonies of P. pouchetii

D Estep et al. (1990)

Low feeding by nauplii on some cell types of P. globosa Dutz and Koski (2006)

Low reproductive output from Acartia spp., Temora longicornis, Pseudodiaptomus pelagicus and Eucalanus pileatus feeding on Phaeocystis, despite sometimes high ingestion rates.

E Klein Breteler and Koski (2003), Long and Hay (2006), Tang et al. (2001), Turner et al. (2002), Verity and Smayda (1989)

Inhibiting copepod feeding by transparent exopolymer particles (TEP) derived from a Phaeocystis globosa.

Dutz et al. (2005)

Suggested reduction of zooplankton feeding due to mucus secretion from colonies of P. globosa.

Seuront et al. (this volume)

Not a good food organism for the barnacle Balanus balanoides Cook and Gabbott (1972)

Other organisms

Oxygen deWciency due to sedimenting Phaeocystis killing less mobile fauna in the sediments.

Rogers and Lockwood (1990)

Colonies clogging gills and thus reducing feeding in several mussels, especielly smaller, e.g., P. globosa colonies reduced feeding in Mytilus edulis <3 cm, while larger where able to Wlter colonies.

Blauw (this volume), Kopp (1978), Meixner (1981), Petri et al. (1999), Pieters et al. (1980), Smaal and Twisk (1997)

Inhibited growth in the bryozoan Electra pilosa possibly due to Phaeocystis.

Jebram (1980)

Toxic to sea urchin larvae Hansen et al. (2003, 2004)

Toxic to blowXies (Calliphora omitoria) Stabell et al. (1999)

123


occurs. These results were also supported by Levin-sen et al. (2000), who reported ingestion of single P.pouchetii by the smaller females of C. Wnmarchus butnot by the larger C. glacialis and C. hyperboreus.Also, the krill Euphausia superba (35–40 mm)showed similar feeding on 50–100 �m P. antarcticacolonies compared to the diatom Thalassiosira ant-arctica, whereas both single cells and larger coloniesof P. antarctica were grazed at lower rates comparedto the diatom (Haberman et al. 2003). Thus, data suchas these support the notion that substantial shifts insize between Phaeocystis life forms aVect grazing by

diVerently sized predators. However, there is still aconsiderable variation in feeding rates on variousforms of Phaeocystis, ranging from zero to expectedmaximum rates (sensu Hansen et al. 1997) for a num-ber of predators (reviewed in Weisse et al. 1994;Schoemann et al. 2005).

In order to evaluate the relative importance of fac-tors other than size and how they may help explainthe observed variations in grazing rates, we compiledthe available quantitative data, converted them intocarbon units, and performed a series of correspon-dence and cluster analyses described below.

Table 2 continued

Notes:

A: It has also been reported that the high concentrations of acrylate in Phaeocystis colonies do not inhibit surrounding bacteria and maybe absorbed to the mucus matrix (Noordkamp et al. 2000)

B: But when solitary cells are abundant during blooms (Admiraal and Venekamp 1986; Weisse and ScheVel-Möser 1990), or duringthe breakdown (van Boekel et al. 1992), microzooplankton such as ciliates may be numerous

C: There are also some reports on apparently increased abundances of mesozooplankton during periods of blooms of Phaeocystis(Fransz and Gieskes 1984; Fransz et al. 1992; Weisse et al. 1986)

D: But in a later bloom stage the copeods switch to selectively feed upon the senescent P. pouchetii, rather than the diatoms (Estepet al. 1990)

EVect Note References

Migrating herring hindered by a “barrier” of Phaeocystis blooms

F Savage (1930, 1932)

Toxic to cod larvae Aanesen et al. (1998), Eilertsen and Raa (1995), Hansen et al. (2004)

Skin and eye irritation of humans Dunne et al. (1984)

Table 3 Quantitative laboratory studies on protozooplankton grazing on Phaeocystis

All experiments are based on particle disappearance and cell counts of cultured P. globosa, or cf. globosa in Hansen et al. (1993). Notesare given on whether the grazer feed (yes) or not at all (no) on Phaeocystis, or showed higher or lower feeding rates on Phaeocystis,compared to alternative prey oVered in parallel single prey species incubations

Grazer Alternative prey Feeding on P. globosa References

Oxyrrhis marina No Yes Hansen et al. (1993)

Strombidinopsis acuminatum No Yes Hansen et al. (1993)

Strombidium elegans No No Hansen et al. (1993)

Strombidium sp. No Yes Verity (2000)

Noctiluca scintillans No Yes Jakobsen and Tang (2002)

Gyrodinium dominans No Yes Tang and Simó (2003)

Lohmanniella oviformis Isochrysis galbana Lower Tang et al. (2001)

Rimostrombidium conicum Isochrysis galbana Higher Tang et al. (2001)

Strombidium vestitum Isochrysis galbana Higher Tang et al. (2001)

Gyrodinium dominans Isochrysis galbana Higher Tang et al. (2001)

Gymnodinium sp. Isochrysis galbana Lower Tang et al. (2001)

Mesodinium pulex Gymnodinium sp. No Tang et al. (2001)

123


Tab

le4

Lite

ratu

re i

nfer

ring

qua

ntita

tive

evid

ence

of

mic

rozo

opla

nkto

n co

mm

unit

y gr

azin

g (g

) an

d gr

azin

g im

pact

(pe

rcen

tage

of

aver

age

stan

ding

sto

ck (

SS)

rem

oved

d¡

1 ) on

Pha

eocy

stis

sol

itary

cel

ls in

nat

ural

pla

nkto

n

Spe

ciW

c ph

ytop

lank

ton

grow

th ra

te (�

) is

also

sho

wn.

All

rat

es a

re q

uant

iWed

by

the

dilu

tion

tech

niqu

e (L

andr

y an

d H

asse

tt 1

982)

. Pre

y co

ncen

trat

ions

wer

e an

alyz

ed b

y ce

ll co

unts

,to

tal c

hlor

ophy

ll a

frac

tion

s (T

otal

Chl

a),

hig

h-pe

rfor

man

ce li

quid

chr

omat

ogra

phy

(HPL

C),

or X

ow c

ytom

etry

(F

C)

A: I

ncub

atio

n ti

me

only

5–1

4h

duri

ng th

e da

y

B: I

nsta

ntan

eous

gra

zing

(g)

max

·0.

1d¡

1 w

hen

the

phyt

opla

nkto

n w

as d

omin

ated

by

Pha

eocy

stis

C: A

dditi

onal

exp

erim

ent w

ith F

LA

(C

hlor

ella

). O

nly

5 of

13

test

ed c

ilia

tes

inge

sted

the

labe

led

phyt

opla

nkto

n

D: A

lso

mea

sure

d di

met

hyl s

ulph

ide

(DM

S)

dyna

mic

s. D

urin

g P

. pou

chet

ii b

loom

g w

as 0

.0 a

nd 0

.3

E: N

o no

tes

on s

peciW

c P

haeo

cyst

is r

ates

Pha

eocy

stis

spp

.A

rea

Tim

eA

naly

sis

� (d

¡1 )

g (d

¡1 )

Impa

ct (

% S

S d-1

)N

ote

Ref

eren

ces

ME

SOC

OSM

(na

tura

l pla

nkto

n in

door

tank

)

glob

osa

Sou

th N

orth

Sea

Sep

Cel

l Cou

nts

?–

0.3

–?

0.3–

0.7

26–4

8B

russ

ard

etal

. (20

05)

FIE

LD

cf. g

lobo

sa?

Sou

th N

orth

Sea

Apr

–May

Cel

l Cou

nts

0.8–

2.3

0.9–

4.2

59–9

8A

Wei

sse

and

ScheV

el-M

öser

(19

90)

cf. g

lobo

sa?

Sou

th N

orth

Sea

Feb–

Jul

Tot

al C

hl a

¡0.

3–0.

40.

0–0.

60–

46B

Bru

ssar

d et

al. (

1995

)

glob

osa

Sou

th N

orth

Sea

Apr

ilT

otal

Chl

a0.

1–0.

70.

3–1.

124

–68

Stel

fox-

Wid

dico

mbe

eta

l. (2

004)

pouc

heti

iN

orth

Nor

way

fjo

rdA

pril

Tot

al C

hl a

0.3–

0.5

0.21

–0.3

619

–30

CA

rche

r et

al. (

2000

)

pouc

heti

iL

abra

dor

Sea

May

–Jun

Tot

al C

hl a

0.2–

0.9

0.0–

0.3

0–27

DW

olfe

eta

l. (2

000)

anta

rcti

caR

oss

Sea

Oct

–Apr

Chl

a H

PL

C F

C?

0–0.

230–

21E

Car

on e

tal.

(200

0)

anta

rcti

caA

ntar

ctic

aN

ov–M

arC

hl a

HP

LC

FC

0.1–

0.6

0.1–

0.3

14–2

6E

Lan

dry

etal

. (20

02)

anta

rcti

caA

ntar

ctic

aD

ecC

hl a

HP

LC

FC

0.2–

0.9

0.1–

1.0

10–6

3E

Selp

h et

al. (

2001

)

123


Treatment of literature data

Many reports of crustacean grazing on Phaeocystisspp. are based on non-prey-speciWc gut Xuorescenceduring blooms of Phaeocystis. An unknown fractionof such Xuorescence may stem from prey other thanPhaeocystis. Indeed, the often co-occurring diatomsmay even be a preferred prey (Gasparini et al. 2000).In addition, more than half the total biomass (andchlorophyll) of the Phaeocystis colony may be due todiatoms and other organisms living in and on the col-onies during late bloom stages (Sazhin et al. this vol-ume). Therefore, we exclude data based on non-speciWc gut pigments of grazers feeding on mixed ornatural food suspensions. We converted all grazingrate measurements into common currency of carbonunits, using either (in the preferred order): (1) directlyreported data, (2) data reported in accompanyingpapers, (3) personal communications with theauthors, or (4) common conversion factors (such asthose used in Hansen et al. 1997). For quantitativeand statistical analyses we included only grazing datafrom studies that reported experiment location (Weldor laboratory study), grazer species, stage or size, andPhaeocystis average size (or size range). To beincluded in the statistical analysis the sources alsomust have reported Phaeocystis species, abundance,morphotype and growth state (exponential or station-ary—either given in the text or assumed from thestate of the bloom). See Table 5 for further details onthe variables. The sources used are listed in Table 6.

Statistical methods

To investigate relationships between crustacean graz-ing rates on Phaeocystis and experimental conditions,a multiple correspondence analysis (MCA) followedby a hierarchical cluster analysis (HCA) was per-formed using SPAD 3.5 software (Lebart et al. 1988).The combination of MCA and cluster analysis is acommon way to explore relationships among a largenumber of variables and to facilitate interpretation ofthe correspondence analysis results (Lebart et al.2000). MCA uses a contingency table as data, whichprovides a simultaneous representation of the obser-vations (rows) and variables (column) in a factorialspace. This form of multivariate analysis describesthe total inertia (or variability) of a multidimensional

Table 5 Active structural variables used in the multiple corre-spondence analysis (MCA). n denotes the number of observa-tions from each source

Description of variables: modalities Label n

Experiment location

Field Field 91

Laboratory Laboratory 205

Crustacean predators

Acartia clausi Acl 13

Acartia hudsonica Ahu 5

Acartia tonsa Ato 12

Pseudocalanus elongatus Pel 13

Temora longicornis Tlo 35

Temora stylifera Tst 15

Metridia longa Mlo 1

Centropages hamatus Cha 14Calanus Wnmarchicus CW 105

Calanus glacialis Cgl 8

Calanus hyperboreus Chy 75

Phaeocystis species

globosa P. globosa 107

pouchetii P. pouchetii 189

Phaeocystis growth

Exponential Exponential 277

Stationary Stationary 19

Phaeocystis abundance (Ab, �g C l¡1)

0.1–125 Ab1 81

125–250 Ab2 91

250–500 Ab3 37

500–1000 Ab4 71

1000–1810 Ab5 16

C-speciWc ingestion (CI, d¡1)

0–0.01 CI1 83

0.01–0.1 CI2 151

0.1–1.5 CI3 62

Phaeocystis selection

Positive selection For 14

Negative selection Against 76

Null selection Null 5

Single prey Single 201

Predator-to-prey size ratio (P:p)

0.8–4 P:p1 57

4–16 P:p2 90

16–64 P:p3 49

64–256 P:p4 25

256–1120 P:p5 75

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set of data, in a sample of fewer dimensions (or axes)that is the best summary of the information containedin the data (Greenacre 1984; Everitt and Dunn 2001).Our data set contains both categorical and continuousvariables that were used in the MCA as active(Table 5) and illustrative variables (PL, ESD, CI andAb deWned below), respectively. The factorial axes ofthe MCA were computed using active (categorical)variables whereas the continuous illustrative (or sup-plementary) variables were simply projected into thisfactorial plane without participating in its computa-tion. The location of these continuous illustrativevariables, is shown as arrows along the factorial axesin Fig. 1A, and expresses their linkage to the patternof the categorical active variables displayed by thefactorial axes (Lebart et al. 2000). Observations withmissing data for carbon-speciWc ingestion and experi-mental characteristics were excluded from the MCA.Only four observations with Phaeocystis antarticawere available, and were therefore also excluded. Adata matrix of the remaining 296 observations witheight active and four illustrative variables were usedfor the analyses (Table 5). The size of predators (pro-some length; PL) and prey (equivalent sphericaldiameter; ESD) were treated as illustrative variables.

These continuous variables were used to calculate apredator-to-prey size ratio (P:p) with Wve categories(or modalities) used in the statistical treatment. Simi-larly, C-speciWc ingestion (CI) and Phaeocystis abun-dance (Ab) were transformed into categoricalvariables of three and Wve categories, respectively, tobe tested both as illustrative and active variables inthe MCA. The metric used in the MCA is based onthe �2. This was also the metric used in the followingcluster analysis. The type of HCA used here is anagglomerative clustering, i.e., a procedure that suc-cessively groups the closest objects into clusters,which then are grouped into larger clusters of higherrank (Legendre and Legendre 1998). The programmeidentiWes: (i) the cluster (group of observations)which has the smallest within-group variance and thegreater variance between groups, and (ii) the descrip-tors (variables) that are highly representative of eachcluster. The descriptors of the observations used inthe clustering were their factorial coordinates on theWrst six axes obtained in the MCA. These Wrst sixaxes explained about 58% of the total variability(inertia) in the data, and the additional amount ofvariability explained by the axes decreased markedlyafter the Wrst six axes.

Table 6 Sources of data used for the multiple correspondence analysis (MCA) and hierarchical cluster analysis (HCA) presented in Fig. 1, and quantitative summary in Fig. 2, respectively

References Location Phaeocystis Fig. 1n

Fig. 2n

Antajan unpublished Field globosa 6 6

Dutz and Koski (2006) Lab globosa 7 7

Estep et al. (1990) Field pouchetii 25 25

Gasparini et al. (2000) Field globosa 55 55

Haberman et al. (2003) Lab antartica 3

Hansen et al. (1990) Lab pouchetii 62 62

Hansen et al. (1993) Lab globosa 5 5

Hansen et al. (1994b) Lab pouchetii 20

Huntley et al (1987) Lab pouchetii 4 4

Klein Breteler and Koski (2003) Field globosa 4

Koski et al. (2005) Field globosa 2 6

Koski unpublished Field pouchetii 3 3

Tande and Båmstedt (1987) Lab pouchetii 95 95

Tang et al (2001) Lab globosa 4

Turner et al. (2002) Lab globosa 15 15

Verity and Smayda (1989) Lab globosa 9 9

Verity (2000) Lab globosa 8 12

Weisse (1983) Lab globosa 18

n denotes the number of observations from each source

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Results from statistical analysis

The result of the MCA indicated that the Wrst and sec-ond axes accumulate about 19% and 12% of the totalvariability, respectively (Fig. 1A). Two variablesbasically contribute to the Wrst axis: the selection

(“Against” and “Single”, cumulated 18% of the con-tribution to axis 1) and the experiment location(“Lab” and “Field”, cumulated 17.5% of the contribu-tion). Thus, this axis diVerentiates laboratory experi-ments where Phaeocystis was the only prey(“Single”), as opposed to Weld experiments where

Fig. 1 First factorial plane of MCA of data on crustacean graz-ing experiment on Phaeocystis. (A) Projections of continuousillustrative variables in the correlation circle (radius 1) and ordi-nation of active variables: Phaeocystis species (�), growth (C)and abundance (�), crustacean species (�), predator-to-prey

size ratio (B), experiment location (�), selection (�). (B) Ordi-nation of data (�) labelled according to their C-speciWc inges-tion characteristic and delimitation of the four groups designedby the hierarchical clustering (�2 distance). See Table 5 for labelidentiWcation

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alternative prey were available and Phaeocystis wasselected against (“Against”). The predator-to-preysize ratio modality “P:p1” (size ratio < 4) also has animportant contribution to the Wrst axis (10%), show-ing that small copepods (such as Centropages hama-tus, Acartia clausi and Pseudocalanus elongatus)tend to reject Phaeocystis in situ. On axis 2, the twomodalities “Stationary” and “For” have the greatestcontribution (18% and 20%, respectively). This axisseparates grazing experiments where Phaeocystis in astationary growth phase was selected positively bypredators in situ. In the Wrst factorial plane we alsoobserved that Phaeocystis concentration and preda-tor-to-prey size ratio in lab experiments were higherthan what was generally observed in situ (Fig. 1A)and that higher carbon-speciWc ingestions weremostly related to laboratory experiments (Fig. 1B).

The combined analysis of the MCA and HCAclearly distinguished four groups of observations(Fig. 1B and Table 7). Groups 1 and 2 bring together97% of the grazing experiments performed in the Weldand are separated from groups 3 and 4, which com-prise 96% of the lab experiments with Phaeocystisprovided as single prey. Group 1 consists of Weldexperiments with small-size copepods selectingagainst P. globosa. Group 2 includes all Weld experi-ments with positive selection for P. pouchetii (93% of

the group), and is characterized by a slightly higherpredator-to-prey size ratio (87% of them had a P:p-ratio of 4–16, “P:p2”). In these experiments Phaeo-cystis was in the stationary growth phase and in rela-tively low abundance (“Ab1” = abundance between0.1 and 125 �g C l¡1). The group 3 is characterizedby lab grazing experiments of Temora spp. onP. globosa. The predator-to-prey size ratio in theselaboratory experiments was higher (89% of them hada P:p ratio of 64–256, “P:p4”) than what was com-monly observed in grazing experiments on naturalplankton. Similarly we observed higher carbon-spe-ciWc ingestion than what was observed in situ for thiscopepod genus (group 1). Group 4 brings together thelab grazing experiments on P. pouchetii by largercopepods (Calanus spp.). This group includes thehighest Phaeocystis abundance and predator-to-preysize ratio tested in lab experiments and grouped thehighest carbon-speciWc ingestion estimates.

In conclusion, the MCA and the HCA analysessuggested that: (1) the lowest grazing rates from theWeld (often zero) were recorded for small copepods(Acartia, Pseudocalanus, Temora and Centropages)in blooms of Phaeocystis globosa colonies, (2) largecopepods (e.g., Calanus) feeding on Phaeocystispouchetii had higher grazing rates, especially in labstudies, when no alternative food was present and (3)

Table 7 Characterization of the most typical properties of the four groups designed by the hierachical cluster analysis deWned inFig. 1 panel B

Gr/mod corresponds to the percentage of the modality belonging to the group, and mod/gr corresponds to the percentage of the groupbelonging to the modality. Modality label as in Table 5. n denotes the number of observations

Group n 1 2 3 4

82 15 27 172

Modality gr/mod mod/gr Modality gr/mod mod/gr Modality gr/mod mod/gr Modality gr/mod mod/gr

Group characteristics

Against 95 88 For 100 93 P:p4 96 89 Single 84 98

Field 80 89 Stationary 79 100 Tst 100 56 P. pouchetii 87 95

P:p1 96 67 Ab1 19 100 P. globosa 25 100 Lab 82 98

P. globosa 66 87 Field 16 100 Tlo 34 44 P:p5 100 44

CI1 55 56 P:p2 14 87 Lab 13 100 Chy 96 42

Cha 100 17 Cgl 38 20 CI3 19 44 CW 88 53

Acl 100 16 P. pouchetii 7 93 Ab4 86 35

Pel 100 16 Exponential 62 100

Ab1 48 48 P:p3 88 25

Tlo 63 27 Ab5 100 9

Ab2 44 49 CI3 77 28

CI2 66 58

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P. pouchetii in a stationary growth phase was posi-tively selected by large copepods.

It is important to note that grazing data for largecopepods (Calanus spp. and Metridia longa) wereonly available for P. pouchetii, whereas grazing stud-ies with small copepods (Acartia, Centropages,Pseudocalanus and Temora) were limited to P. glob-osa. Thus, the presently available data do not allow usto determine whether the diVerent results for P.pouchetii and P. globosa are due to diVerencesbetween the two species, or diVerences between thepredators. In order to test for species-speciWc diVer-ences, we need to compare grazing on both speciessimultaneously using similar methodologies in futurestudies.

Quantitative results from data on crustacean grazing

Because the statistical analysis suggested a largediVerence between feeding rates in laboratory andWeld investigations, we compared the average speciWcingestion rates in all available Weld and laboratoryexperiments (Table 6), and for Wve groups of preda-tor-to-prey size ratios separately (Fig. 2). These com-parisons revealed that: (1) overall feeding (carbonspeciWc ingestion) on Phaeocystis spp. was signiW-cantly lower [p < 10¡8, analysis of variation(ANOVA)] in all Weld (average 2.5% d¡1) studieswith natural plankton, compared to laboratory studies(average 11% d¡1), (2) the highest average carbon-speciWc ingestion rate (23% d¡1) on Phaeocystis spp.was found when the predator-to-prey size ratio (P:p)was 4–16 in lab studies, whereas there was no clearsize ratio trend in Weld studies, and (3) ingestion waslow (·2% d¡1) when P:p was < 4 in both lab andWeld, indicating that the upper eVective size limit forprey equivalent spherical diameter was ¼ of the pred-ator prosome length.

Thus, crustacean grazers show a much lower graz-ing on Phaeocystis in the Weld than in the laboratory.One reason for this discrepancy could be that fewerthan 5% of the laboratory studies oVered the cope-pods alternative prey to Phaeocystis whereas alterna-tive prey were available in the Weld. Alternatively,laboratory cultures might not display the same chemi-cal grazing cues (and possible grazing deterrents) asPhaeocystis growing in natural plankton. Hapto-phytes may lose their inhibitory eVects in vitro, andtoxicity may be species-, strain- or growth-condition-

speciWc (Edvardsen and Paasche 1998). Support forthis hypothesis comes from laboratory studies thatfailed to recreate toxicity in the lab that was observedin the Weld, even with haptophytes isolated fromhighly toxic blooms, such as the Chrysochromulinapolylepis bloom in 1988 (Nielsen et al. 1990). Like-wise, the antipredation eVect revealed by Estep et al.(1990) in actively growing Weld-collected Phaeocys-tis pouchetii apparently disappeared during the Wrst12 h in experimental containers. It may be that labora-tory or other in vitro studies underestimate the nega-tive eVects of potentially toxic haptophytes in situ,but this requires explicit evaluation.

Ideally, future investigations on the ecology ofzooplankton feeding should preferably be conductedin situ, although laboratory experiments are needed toinvestigate the eVects of potentially important signal-ing substances between Phaeocystis and diVerent pre-dators in presence of realistic alternative prey.

Grazing by protozooplankton and other microzooplankton

General trends in grazing by protozoan microzooplank-ton on Phaeocystis are diYcult to assess since thenumber of quantitative investigations is limited(Tables 3 and 4). Very few studies have investigated

Fig. 2 Crustaceans (all stages of copepods and krill) grazing onPhaeocystis pouchetii, P. globosa or P. antarctica, in laboratoryand Weld experiments. Average daily carbon-speciWc ingestionrates (percent �g C �g C¡1 d¡1) are presented for Wve diVerentpredator-to-prey size categories [derived from predator prosomeor carapace length and average equivalent spherical diameter(ESD) of the Phaeocystis prey, solitary cells or colonies]. Errorbars denote the standard error (SE) of the average; the numberof observations (n) for each category are given above each col-umn. Note the high daily ration for P:p size ratio 64–256 in theWeld is due to a single (30%) value (with that value excluded, therate is 3.0 § 1.0 %)

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microzooplankton as potential grazers on colonialPhaeocystis spp. The colonies are protected by a toughskin (Hamm et al. 1999) and microzooplankters aregenerally assumed to be too small to prey actively oncolonial forms of Phaeocystis (Hansen et al. 1994a;Weisse et al. 1994; Tang 2003). In accordance, Irigoienet al. (2003) reported that nauplii of Calanus Wnmar-chicus did not ingest colonies of Phaeocystis in theIrminger sea. However, the protists Noctiluca scintil-lans (Weisse et al. 1994; Jakobsen and Tang 2002) andapparently Gyrodinium cf. spirale (Stelfox-Widdi-combe et al. 2004) are able to ingest small colonies,while some tintinnids and rotifers “attack” and “hoveraround colonies”, possibly ingesting released cells(Hollowday 1949; Admiraal and Venekamp 1986). Theabundance of microzooplankton has also been reportedto decline or remain low during natural blooms of colo-nial Phaeocystis, but increases rapidly during thebreakdown of the colonies at the end of the bloom (e.g.,Peperzak et al. 1998; van Boekel et al. 1992). This sug-gests that actively growing colonies are inferior preyfor microzooplankton, while single cells released fromdecaying colonies may be a suitable food source. How-ever, an alternative explanation for the low microzoo-plankton abundance during Phaeocystis blooms is thestrong selective predation pressure from larger zoo-plankton such as copepods (Hansen et al. 1993; Gaspa-rini et al. 2000).

It is clear from the literature that at least somemicrozooplankton may readily ingest single-celledPhaeocystis (Tables 3 and 4), and chemical cues frommicrozooplankton grazing have been shown to inducecolony formation (Long and Hay 2006) and enlarge-ment in P. globosa (Tang 2003), supporting the

assumption that microzooplankton graze on the singlecells but not the colonies. However, some of thereported grazing rates in laboratory studies were low,with or without alternative prey present (Table 3).Also, in several incubation experiments with naturalplankton the microzooplankton community grazingrates were very low (·0.1 d¡1) during dominance ofPhaeocystis (Table 4). It is well known that somemicrozooplankton feed selectively (e.g., Verity 1988;González et al. 1990; Strom and Loukos 1998; Archeret al. 2000), and it was recently shown that copepodnauplii ingest some clones and cell morphotypes of P.globosa at low rates (Dutz and Koski 2006). Resultsshowing selection against single cells by microzoo-plankton in the sea was obtained in recent dilutionexperiments in the English Channel (Table 8). Theseexperiments yielded zero or close to zero microzoo-plankton grazing rates on single-celled P. globosa, buthigh microzooplankton grazing rates on diatoms basedon cell counts, while bulk measurements of chlorophylla (as used in most of the experiments in Table 4) indi-cated intermediate grazing values. This suggests thatmicrozooplankton feeding on Phaeocystis may behighly variable in the sea, and reliable grazing ratemeasurements will therefore require taxon-speciWcquantitative methods, rather than bulk measurements(see further discussion under Future challenges).

Cell-type and life-stage-speciWc interactions with grazers

In the species P. globosa, three solitary, Xagellatedcell types (micro-, meso, and macroXagellates)

Table 8 Microzooplankton grazing on Phaeocystis globosa solitary cells during blooms in the English Channel oV northen FranceMay 2003 and April 2004 (JC Nejstgaard, AF Sazhin and LF Artigas unpubl.)

Dilution experiments were performed and analyzed as decribed in Nejstgaard et al. (2001). SpeciWc phytoplankton growth rate (�),microzooplankton grazing coeYcient (g), grazing impact (percentage of average standing stock removed d¡1 ). §SE for the mean.* p < 0.05, ** p < 0.01, and *** p < 0.001 for � or g = 0. Prey types are given with equivalent spherical diameter size ranges (�m)

Date Prey type (�m) r2 � (d¡1) G (d¡1) Grazing impact (% SS d¡1)

Apr 2003 Chl a (>0.45) 0.58 0.24 § 0.07** 0.61 § 0.14 *** 46

Diatoms (5-99) 0.45 1.34 § 0.18*** 1.24 § 0.40** 71

Phaeocystis (2-8) 0.04 0.08 § 0.16 ns 0.21 § 0.30 ns 19

May 2004 Chl a (>0.45) 0.13 ¡1.17 § 0.12*** 0.18 § 0.18 ns 17

Diatoms (5-99) 0.18 0.16 § 0.09 ns 0.19 § 0.13 ns 18

Phaeocystis (2-8) 0.04 ¡1.14 § 0.20 *** ¡0.23 § 0.34 ns 0

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diVering in size and morphology have been described(Kornmann 1955; Peperzak et al. 2000). The ecologi-cal roles of these diVerent cell types are largelyunknown, partly due to diYculties in the identiWca-tion and quantiWcation of the Xagellated cell type inWeld samples (Rousseau et al. 1994; Peperzak et al.2000; Schoemann et al. 2005; Rousseau et al. thisvolume). A recent study showed that the grazing mor-tality of single cells may depend on the cell type, withmoderate to high ingestion by Temora longicornisnauplii on non-Xagellated cell types, but rejection of aXagellate type (Dutz and Koski 2006). This rejectionwas ascribed to the production of chitinous threadsand the cohesion of threads into pentagonal star-likestructures which are a typical feature of mesoXagel-lates (Chretiennot-Dinet et al. 1997; Peperzak et al.2000).

The variable cell-type-speciWc grazing mortality ofP. globosa oVers important insight into the naturalhistory of this phytoplankton species. Although Xag-ellated and non-Xagellated cell types co-occurthroughout the year, blooms of Phaeocystis in tem-perate waters are generally dominated by the colonialcell type and by colonies (Peperzak et al. 2000; Rous-seau et al. this volume). At the end of such blooms,single cells are released from the colonies presumablydue to nutrient deWciency or irradiance limitation. Theliberated cells appear to suVer a high mortality due tomicrozooplankton grazing, cell lysis and/or perhapssedimentation (van Boekel et al. 1992; Brussaardet al. 1995; Riebesell et al. 1995; Brussaard et al. thisvolume; Reigstad & Wassmann this volume). Con-current to the liberation and disappearance of singlecells, an increasing abundance of micro/mesoXagel-lates has been observed in mesocosms and in the Weld(Veldhuis et al. 1986; Peperzak et al. 2000; Escara-vage et al. 1995; Nejstgaard et al. 2006). The forma-tion of intracolonial Xagellated cells may bridge thedisappearance of colonial cells and the appearance ofXagellated cells (Peperzak et al. 2000). These haploidmicro/mesoXagellates probably function as gametesor spores to survive unfavourable conditions duringthe warm summer months (Veldhuis et al. 1986;Peperzak et al. 2000). Reduced vulnerability of thesecells to microzooplankton grazing could explain theaccumulation of single Xagellated cells despite a highgrazing pressure at the end of Phaeocystis blooms,and be part of these phytoplankters’ strategy toincrease survival and foster bloom formation when

favorable conditions return. Future studies shouldinvestigate the relevance of cell type- and life-stage-speciWc selection on wider range of zooplanktonorganisms.

Colony formation and its potential rolein morphological defense

The presence of the two distinctly diVerent morpho-types in Phaeocystis has long intrigued scientists, andmuch remains unknown about their respective biolog-ical roles and regulation of transition between mor-photypes (Rousseau et al. 1994; Lancelot et al. 1998;Rousseau et al. this volume). The prevalence of bothmorphotypes in natural Phaeocystis blooms in con-trasting water types prompts the idea that Phaeocystiscolony development is regulated by common factors(Lancelot and Rousseau 1994) and contributes to thesuccess of the genus in marine systems (Rousseauet al. 1994; Lancelot et al. 1998; Rousseau et al. thisvolume). The production of the mucilaginous struc-ture represents a substantial energy investment by thecells; the mucilaginous matrix may account for >50%of the total organic carbon of a Phaeocystis popula-tion (Rousseau et al. 1990; Mathot et al. 2000). Thelarge colony size may also pose a problem of diVu-sion limitation to nutrient and oxygen uptake,although a modeling study shows that the colonies areunlikely to be limited by diVusion (Ploug et al. 1999).Thus, compared to solitary Phaeocystis cells, it islikely that the formation of colonies involves someadditional costs, but that the drastic increase in sizemay be an eVective defense mechanism against (rela-tively) small grazers, not unlike the highly successfulfreshwater colonial chlorophyte Scenedesmus (Lür-ling 2003; e.g., Lürling and Van Donk 1997), cyano-bacteria Microcystis aeruginosa and Sphaerocystissp. (e.g., De Bernardi and Giussani 1990), and fordiVerent copepods feeding on the large colony-form-ing diatom Thalassiosira partheneia (Schnack 1983).

Some studies suggest that microzooplankton preferand perform better on single cells than on colonies.When incubated with a mixture of Phaeocystis glob-osa single cells and colonies, microzooplanktonreduced the single cells to very low abundance, andthe grazer population subsequently declined evenwhen colonies were abundant, presumably due tostarvation (Jakobsen and Tang 2002). When restricted

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to a single diet of either single cells or colonies, theciliate Euplotes grew three times faster on single cells(Long 2004). In contrast, the copepod Acartia tonsaand mixed mesozooplankton had higher feeding rateson colonies compared to single cells (Long and Hay2006). The diVerential susceptibility of morphologiesto grazers could allow Phaeocystis to use transforma-tions as an adaptive, inducible response towards graz-ers. Two recent studies tested the role of chemicalcues for inducing transformations using either incuba-tors separated by a permeable membrane (Tang 2003)or Wltrate experiments (Long 2004). In one studychemical cues from grazers triggered colony enlarge-ment (Tang 2003). In the other study microzooplank-ton cues enhanced colony formation while cues frommacrozooplankton suppressed colony formation(Long 2004). These observations point to the involve-ment of a grazing-related chemical signal in morpho-logical defense, but the chemical characteristics ofthis signal remain unknown (Long and Hay 2006;Tang 2003). Colony formation by Phaeocystis couldaVect grazing even after the demise of a bloom. Forexample, the degrading colony matrix, making thesurrounding water gelatinous, may continue to pre-vent grazing losses of single cells by microzooplank-ton (Seuront et al. this volume), and similarly,transparent exopolymer particles formed by coagula-tion of colony-derived carbohydrates could alsoinhibit copepod grazing (Dutz et al. 2005).

Chemical defense

Macroalgae commonly use chemical defense againstgrazers (Hay and Fenical 1988; Pohnert 2004), andsimilar examples may exist in phytoplankton (seereview by Pohnert 2004; and further examples inYoshida et al. 2004; Pohnert 2005). A few observa-tions suggest that chemical defense could be impor-tant for survival of Phaeocystis during exponentialgrowth (Weisse et al. 1994; Estep et al. 1990; Longand Hay 2006). Recently, a number of toxins havebeen isolated from Phaeocystis (reviewed by vanRijssel et al. this volume), and Phaeocystis is report-edly toxic to some aquatic organisms, including phy-toplankton, sea urchin and cod larvae (Table 2).However, speciWc chemical zooplankton feedingdeterrents from Phaeocystis have not yet been iso-lated and characterized so their existence is still

hypothetical. Several of the reported toxic eVectswere obtained using organisms (or even extracts) thatdo not interact in nature, and the ecological relevanceof such results is unknown.

Does DMS aVect grazing on Phaeocystis?

Phaeocystis is a prominent producer of the secondarymetabolite dimethylsulphoniopropionate (DMSP)that can be enzymatically cleaved to acrylate and thevolatile trace gas dimethyl sulphide (DMS; Kelleret al. 1989; Schoemann et al. 2005; Stefels et al. thisvolume). DMSP is a multifunctional compound thatprobably assists several physiological processesrelated to salinity-, temperature- and light-stress inalgal cells (Stefels 2000). This compound and itscleavage products have also been suggested to func-tion as grazing deterrents (Strom et al. 2003; Wolfeet al. 1997) and it is possible that they provide a com-petitive advantage to Phaeocystis when non-DMSP-producing alternative prey are available to potentialpredators. Microzooplankton grazing greatlyincreases the production of DMS in Emiliania huxleyi(Wolfe and Steinke 1996) and microzooplankton aresuspected to have caused the conversion of Phaeocys-tis-DMSP to DMS in the southern North Sea (Archeret al. 2003). The grazing-induced production of DMSmay be analogous to the production of volatile info-chemicals during herbivore grazing on terrestrialplants that utilize such trace gases to attract carni-vores (Dicke and Sabelis 1988; Steinke et al. 2002;Hay et al. 2004). Such indirect defense mechanismsinvolve interactions on three trophic levels thatinclude plants, herbivores and carnivores. Seabirdsare attracted by gradients of DMS in the atmosphere(Nevitt et al. 1995; Nevitt and Bonadonna 2005), andcopepods are chemosensitive to DMS and react withsearch behavior when encountering plumes of thiscompound (Steinke et al. 2006). If DMS producedduring grazing makes the microzooplankton grazersmore susceptible to predation by copepods, theninvestment into such an indirect defense mechanismcould be beneWcial for the phytoplankton.

However, the ecological consequences of theproduction of DMS and associated compounds arecontroversial and explicit tests of possible defensivefunctions for Phaeocystis are required. For example,Tang and Simó (2003) did not observe negative

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eVects when the heterotrophic dinoXagellate Gyrodi-nium dominans grazed on P. globosa single cells, andthe grazers retained >40% of the ingested DMSP.Furthermore, the grazing-induced production of DMSby unicellular phytoplankton is a result of grazing onindividual cells and, as a consequence, these ingestedcells will not directly beneWt from the potential sig-naling to carnivorous enemies of the microzooplank-ton. It is possible that such indirect defensemechanisms are beneWcial for Phaeocystis popula-tions but they would also be of beneWt to other mem-bers of the phytoplankton community that may notinvest in chemical defenses (the cheater problem:Lewis 1986). One may argue that the cheater problemdoes not exist within a bloom of genetically closelyrelated cells. However, molecular studies have shownthat the genetic variation in phytoplankton popula-tions is high, even within a monospeciWc diatombloom (Rynearson and Armbrust 2005). It is impossi-ble to predict functional diversity from such molecu-lar data and there is very little information on theeVect of genetic variation on the ecophysiologicalWtness in Phaeocystis.

Evidence is accumulating that chemical communi-cation inXuences the composition and dynamics ofpelagic communities (Pohnert 2004). The productionof DMSP in Phaeocystis is probably only one exam-ple where a secondary metabolite beneWts the physi-ology of individual cells and its catabolic productscould aVect the structure and function of Phaeocystis-dominated food webs. This is a complex research areathat needs to be addressed with more detailed studiesin the future.

Does nutritional value aVect grazing on Phaeocystis?

Copepods may feed selectively based on nutritionalquality of the prey (e.g., Houde and Roman 1987).However, it is not clear how food quality of the diVer-ent forms of Phaeocystis aVects zooplankton grazing.It has been suggested that Phaeocystis spp. are of lownutritional value due to their low content of polyun-saturated fatty acids (PUFA) (Al-Hasan et al. 1990;Claustre et al. 1990; Rogers and Lockwood 1990;Nichols et al. 1991; Cotonnec et al. 2001; Tang et al.2001; Turner et al. 2002). This contrasts with the highsurvival and development rates observed in other

studies (Verity and Smayda 1989), at least for somestrains of P. globosa (Dutz and Koski 2006). Highamounts of C18-PUFA were detected in a P. globosabloom in the North Sea (Hamm and Rousseau 2003)and in a P. pouchetii bloom in Balsfjorden in northernNorway (Hamm et al. 2001). The mucus produced bycolonies is generally considered to be of low nutri-tional value, refractory (Thingstad and Billen 1994),and of low carbohydrate content (van Rijssel et al.1997). However, the composition of the mucus mate-rial may vary during a bloom cycle (Alderkamp et al.2006), and colonization of this material by pennatediatoms and other organisms on and inside older colo-nies (Hamm and Rousseau 2003; Sazhin et al. thisvolume) may increase its nutritional value. BesidesPUFA and carbohydrates, the eVects of other impor-tant nutritional components of Phaeocystis such asamino acids, sterols and vitamins, on copepod feedingand reproduction are still poorly known.

Survival of gut passage?

Some phytoplankton can survive gut passage, a traitthat is often overlooked in zooplankton studies. Forinstance, large fractions of the chlorophytes Chla-mydomonas reinhardtii and Selenastrum capricornu-tum survive passing the guts of Daphnia. This isconsidered a defense mechanism by the algae toreduce grazing pressure when their growth rates arelow (van Donk et al. 1997). Further, the colonial chlo-rophyte Sphaerocystis schroeteri survives gut passagein Daphnia and beneWts from grazer-released nutri-ents. This interaction is hypothesized to aVect bloomformation in this species (Porter 1976). If cells ofPhaeocystis may survive gut passage of zooplankton,this would have signiWcant implications for the under-standing of the grazing interactions. Because, netremoval rates of the prey from the population willdecrease, and if cells may produce defense chemicalsupon predation and surviving gut passage it wouldaVect the chemical antipredatory mechanisms sug-gested above. But, to our knowledge there are no suchstudies for Phaeocystis or any other haptophyte phyto-plankton. However, small intact colonies of P. pouch-etii have been observed Xuorescing inside copepodpellets in the Barents Sea (P. Verity and P. Wassmann,personal communication) suggesting that survivinggut passage might be possible for Phaeocystis.

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Conclusions and future challenges

Although over 100 publications have examined zoo-plankton grazing on Phaeocystis spp., more than 90%report on copepods or other crustacean grazers, soquantitative data for other grazers are limited. Graz-ing on Phaeocystis was often determined by feedingon only single types of cultured phytoplankton in thelaboratory. Field reports often do not provide enoughinformation to evaluate even some of the most basicfactors known to aVect zooplankton grazing simulta-neously, such as predator-to-prey size ratio, food con-centration and feeding rates on alternative prey.Further, most reports on crustacean grazing in theWeld are based on non-prey-speciWc grazing estima-tions such as bulk gut pigments, that cannot be used todetermine speciWc feeding on Phaeocystis in themixed natural plankton assemblages.

Nevertheless, our analysis of the present literaturesuggests that: (1) laboratory-derived crustacean graz-ing rates on monocultures of Phaeocystis may havebeen overestimated compared to feeding in naturalplankton communities, and should be treated withcaution; (2) formation of colonies by P. globosaappeared to reduce predation by small copepods (e.g.,Acartia, Pseudocalanus, Temora and Centropages),whereas large copepods (e.g., Calanus spp.) wereable to feed on colonies of Phaeocystis pouchetii; (3)physiological diVerences between diVerent growthstates, species, strains, cell types, and laboratory cul-ture versus natural assemblages may explain most ofthe variations in reported feeding rates; (4) chemicalsignaling between predator and prey may be a majorfactor controlling grazing on Phaeocystis; (5) it isunclear to what extent diVerent zooplankton, espe-cially protozooplankton, feed on the diVerent lifeforms of Phaeocystis in situ.

In the present literature there is a dichotomybetween data showing high feeding rates on both sin-gle cells and colonies of Phaeocystis pouchetii bylarger copepods, especially in the laboratory studies,and avoidance of colonies of Phaeocystis globosa byother smaller copepods in the Weld. This imbalance inbasic quantitative data could initially be remedied byapplying classical bottle incubation methods with arange of predators, preferably using natural planktonin situ, analyzed with methods that resolve the feed-ing rates on the diVerent life forms (and prey sizes) ofdiVerent species of Phaeocystis from alternative prey

types. Such analyses could be done by microscopy(Verity and PaVenhöfer 1996; Båmstedt et al. 2000)corrected for food web cascades (Nejstgaard et al.2001), and/or possibly analyzed by a combination ofmore recent methods such as Xow cytometry (Collierand Campbell 1999; Jonker et al. 2000), computer/video-aided plankton counting devices (See et al.2005), and speciWc molecular probing (Caron 2005)to increase the taxonomic precision. However, theability of chemical cues to rapidly alter colony forma-tion indicates that grazing estimates based on cellcounts could grossly misrepresent actual grazingrates.

For example, zooplankton grazing may induce orsuppress colony formation and enlargement (Tang2003; Long 2004; Long and Hay 2006), and accumu-lating data suggests that chemical signaling betweendiVerent levels of predators of prey can play animportant role inXuencing the dynamics in pelagiccommunities (e.g., reviewed by Pohnert 2004; Yosh-ida et al. 2004). This suggests that chemical signalingin artiWcially increased grazer densities over longincubations could confound data from bottle experi-ments by changing the relative abundance of diVerentlife forms in the grazing bottle due to factors otherthan direct ingestion of the cells. Further, recentresults suggesting that feeding on Phaeocystis mayeven be cell type- or life-stage-speciWc (Dutz andKoski 2006), and that new methods accounting forsuch diVerences are necessary.

Thus, the ideal way to assess feeding on Phaeo-cystis would be a direct quantiWcation of feedingrates on speciWc prey by assessing individual preda-tors that have been feeding undisturbed in situ.Molecular quantitative analysis of the prey in theguts and faecal pellets of the predators could poten-tially achieve this. Such approaches are already com-mon in studies of e.g., terrestrial arthropods(Sheppard and Harwood 2005; Symondson 2002),and it has been shown that prey DNA from hapto-phyte phytoplankton can be detected in copepod gutsand fecal pellets by standard polymerase chain reac-tion (PCR) targeting 18S ribosomal DNA (Nejstg-aard et al. 2003). More recently, it was also shownthat carnivorous diet may be inferred from the con-tent of copepod fecal pellets using standard PCR(Vestheim et al. 2005), and that diVerent phytoplank-ton DNA, including Phaeocystis, may be quantiWedin guts and fecal pellets from both appendicularians

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and copepods using quantitative real-time PCR(Nejstgaard et al. 2005; Troedsson et al. 2007).

Thus the rapidly developing molecular approachesmay help us obtain more-realistic ingestion rates ofPhaeocystis and other live prey in situ. However, tofurther reveal and quantify mechanisms controllingthe complex trophic interactions between Phaeocystisand its predators, new approaches need to be devel-oped. In concert with the recent review by Pohnert(2004) we conclude that such development will prob-ably be as complex as the interactions it tries toreveal. Developing successful innovative approachesand better quantitative analytical tools will dependlargely upon multidisciplinary eVorts between chem-ists, molecular biologists and plankton ecologists.

Acknowledgements We thank S. Gasparini for his valuablesuggestions concerning MCA and HCA analyses. This workwas supported by the Norwegian Research Council project152714/120 30 to JCN, the US-NSF OPP award ANT-0440478to KWT, the UK Natural Environment Research Council grantsNER/I/S/2000/00897 and NE/B500282/1 to MS, the GermanFederal Ministry for Education and Research grants within theGLOBEC Germany project 03F0418C to JD, the CarlsbergFoundation to MK, the Belgian Research Program forsustainable management of the North Sea within the AMOREproject MN/DD/20/21/22 to EA, and the EPA Star FellowshipU-91599501-0 and a National Parks Ecological ResearchFellowship to JDL.

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