Why do biological oceanographers care about planktonic protozoa (i.e., microzooplankton)?

Why do biological oceanographers care about planktonic protozoa (i.e.,

microzooplankton)?

And why should the microbial loop be included in models of pelagic ecology??

Dian J. GiffordGraduate School of Oceanography

University of Rhode IslandNarragansett, RI, USA

[email protected]://gso.uri.edu/faculty/gifford.html

Classical Linear Food ChainClassical Linear Food Chain

Phytoplankton Zooplankton Fish

D.J. Gifford Imaging LaboratoryGraduate School of OceanographyUniversity of Rhode Island

Phytoplankton

Microbial Food WebMicrobial Food Web Metazoan Food WebMetazoan Food Web

CO2CO2CO2CO2

DOCDOCDOCDOC

Protozoa

Bacteria

Zooplankton

?

POCPOC

?

(Sherr & Sherr 1988)D.J. Gifford Imaging LaboratoryGraduate School of OceanographyUniversity of Rhode Island

Fish

Major TaxaMajor Taxa

Nanozooplankton (2-20 m):Nanozooplankton (2-20 m):

Microzooplankton (20-200 m):Microzooplankton (20-200 m):

Heterotrophic flagellates

Ciliates

Heterotrophic dinoflagellates

Ciliates

Heterotrophic dinoflagellates


Ecological Functions of Planktonic ProtozoaEcological Functions of Planktonic Protozoa

Primary Production: retention of functional chloroplasts; mixotrophy

Nutrient Cycling: excretion fuels water column primary production

Grazing: major source of phytoplankton and bacterial mortality

Trophic Coupling: prey of higher trophic levels


Ciliates Containing Plastids or EndosymbiontsCiliates Containing Plastids or Endosymbionts

Location Depth Season% Ciliate

fauna Author

Woods Hole Surface SpringSummer

FallWinter

51472222

Stoecker et al. 1987

Nantucket Sound 0- 9 m Summer 48 Stoecker et al. 1987

Mediterranean Sea Surface Fall 41 Laval- Peuto &Rassoulzadegan 1988

Georges Bank 0- 1% light Summer 39 Stoecker et al. 1990

D.J. GiffordImaging LaboratoryGraduate School of OceanographyUniversity of Rhode Island

StationM. rubra

(ng C f ixed/ h))L. strobila

(ng C f ixed/ h)% Photosynthesis

Total% Photosynthesis

Microplankton

A1 29 20 1 29

A1 71 96 5 14

B1 32 0 6 31

C1 70 71 2 16

C3 0 15 7 >90

Contribution to Water Column PhotosynthesisContribution to Water Column Photosynthesis


(Stoecker et al. 1990)

Log Dry Weight (mg/organism)

Nit

rogen E

xcr

eti

on R

ate

(ug N

/mg D

ry W

eig

ht/

d)

-10 -8 -6 -4 -2 0 2

100

101

102

103

10-1

10-2

10-3

Protozoa

Metazoan Zooplankton

(Caron 1991)


GRAZING

d [Chl]u [Chl]u ( k - a - m - s - g + x ) ~ 0 dt

=

cell division

advection

mixin

g

sinkin

g

gra

zing

horizon

tal terms

k a m s g

Subant arct ic 0.25 0.04 0.05 <0.02 0.15

Subarct ic 0.50 <0.01 ~0.03 0.01 ~0.45

Subt ropicalGyre

1.2 <0.01 <0.01 <0.01 ~1.2

Equat orialUpw el l ing

1.0 0.04 0.02 0.01 0.90

D.J. GiffordImaging LaboratoryGraduate School of OceanographyUniversity of Rhode islandImaging LaboratoryGraduate School of OceanographyUniversity of Rhode Island

(Banse, 1992)

Protozoan Grazing Impact in Pelagic Ecosystems

Location Season% Primaryproduction

consumed d- 1

Author

Washington Coast Fall 17- 52 Landry & Hassett 1982

Halif ax Harbour MarchAprilJ uneAugustNovember

100554740ns

Gif ford 1988 “ “ “ “

North Atlantic Spring (late bloom)Mid- summerSpring (Phaeocystisbloom)Spring (post- bloom)Summer

25290

10041

Weeks et al. 1993Burkill et al. 1993Gif ford et al. 1995 “ “

Celt ic Sea Annual 16- 35 Burkill et al. 1987

Canadian Arctic Summer 40- 100 Paranj ape 1987

Equatorial Pacif ic WinterFall

~10040- 80%

Landry et al. 1995

Subarctic Pacif ic May ~100 Landry et al. 1993


August September January

Microplankton prey category

Cle

ara

nc

e r

ate

(m

l/c

op

ep

od/h

)In

ge

sti

on

ra

te (

ng

C/c

op

ep

od

/h)

0

5

10

1 2 3 4 5 6 7 Chla

1 2 3 4 5 6 7 Chl a 1 2 3 4 5 6 7 Chl a 1 2 3 4 5 6 7 Chl a

1 2 3 4 5 6 7 Chl a 1 2 3 4 5 6 7 Chl a

0

25

75

15

Acartia tonsa Dana

Coastal Gulf of Mexico Gifford and Dagg, 1988

Neocalanus plumchrus MarukawaIn

ges

tio

n r

ate

(ug

C/c

op

epo

d/d

)

CiliatesHet. dionflagellates> 20 umRadiolarians

Het. flagellates & dinoflagellates < 20 um

0

5

10

15

PhytoplanktonTotal

Mean ingestion Maximum ingestion

Subarctic North Pacific

Gifford, 1993

Crest

Southern Flank

Northeast Peak

Jan Feb/Mar Apr May June

0

0.5

1.0

1.0

1.0

0.5

0

0

Phytoplankton Protozooplankton

Fra

ctio

n B

ody

C In

gest

ed

/d

0.5

Georges Bank

Calanus finmarchicus

Gifford and Sieracki, submitted

Inge

stio

n R

ate

(ug

C/c

opep

od/d

)

22 Jan 26 Feb 14 Apr 24 Jun 9 Jul 23 Jul 20 Aug

40

20

30

10

0

Strong upwelling

Relaxed upwelling

Fessenden and Cowles, 1994

Coastal Oregon

Chemical CompositionTaxon C:N Reference

Phytoplankton 6 Parsons et al. 1984

Heterotrophic flahgellates 4 - 7 Goldman et al. 1985Borsheim & Bratbak 1987

Tintinnid ciliates 4 - 5 Verity & Langdon 1984 4 Stoecker & Sanders 1985

Oligotrich ciliatesMixotrophs 4 - 8 Putt & Stoecker 1989Heterotrophs 3 - 4 Putt & Stoecker 1989

Chemical CompositionChemical Constituent Taxon Reference

Lipids PUFAs Ciliates Aaronson & Baker 1961

Kaneshiro et al. 1979Holz & Conner 1987

H dinoflagellates Harrington & Holz 1968H flagellates Holtz & Connor 1987

Fatty acidsH dinoflagellates Holtz & Connor 1987H flagellates Holz & Connor 1987Ciliates Sul & Erwin 1998

Sterols Ciliates Harvey et al. 1997H flagellates Alam et al. 1984

FAAs Ciliates Kaneshiro et al. 1969

Starch H dinoflagellates Holz & Connor 1987

Ciliates Johnson et al. 1995

Significance: Effects on Consumers

Effect Consumer Prey Reference

Enhanced survival Eurytemora affinis Ciliates Berk et al. 1977

Daphnia pulex Ciliates Wickham et al. 1993Daphnia magna Ciliates +

Hflagellates DiBiase et al. 1990Increased growth rate Megacyclops sp. nauplii Hflagellates Abdullahi 1992

Artemia salina Ciliates +Hflagellates Seki 1964

Increased reproduction Acartia tonsa Ciliates Stoecker & Egloff 1987

H dinoflagellates Kleppel & Burkart 1995Eurytemora affinis Ciliates Heinle et al. 1977Acartia clausi H dinoflagellates Breteler et al. 1980

Significance: Effects on Prey Populations

Prey PopulationConsumer Cleared / day (%) Reference

Eurytemora affinis 100 Sheldon et al. 1982

Acartia sp., Oithona sp. 50 Nielsen & Kiorboe 1981

Acartia tonsa 34-200 Dolan 1991

Artemia franciscana 99 Wurtsbaugh 1992

Neocalanus plumchrus 10-26 Gifford & Dagg 1991

Synchaeta littoralis 80 Arnat 1993

Mesozooplankton Taxa Feeding on Microzooplankton

Suspension Feeding Copepods

Acartia clausi (Ayukai 1987; Wiadnyana & Rassoulzadegan 1989; Broglio et al. 2001)Acartia hudsonica (Wiadnyana & Rassoulzadegan 1989)Acartia longiremis (Levinson et al. 2000)Acartia spp. (Batten et al. 2001)Acartia tonsa (Robertson 1983; Gifford & Dagg 1988; Stoecker & Egloff 1989; Jonsson & Tiselius 1990)Calanus finmarchicus (Gifford, submitted; Levinson et al. 2000)Calanus glacialis (Levinson et al. 2000)Calanus hyperboreus (Levinson et al. 2000)Calanus pacificus (Fessenden & Cowles 1994)Calanus propinquus (Atkinson 1995)Calanus spp. (Batten et al. 2001)Centropages typicus (Wiadnyana & Rassoulzadegan 1989)Centropages cherchiae (Batten et al. 2001)Centropages abdominalis (Fessenden & Cowles 1994)Clausocalanus spp. (Batten et al. 2001)Eucalanus pileatus (Verity & Paffenhofer 1996)Eurytemora affinis (Berk et al. 1977)Metridia gerlachei (Atkinson 1995)Neocalanus plumchrus (Gifford 1993)Neocalanus tonsus (Zeldis et al. 2002)Oithona spp. (Atkinson 1995)Pseudocalanus sp. (Fessenden & Cowles 1994)Para-pseudocalanus spp. (Batten et al. 2001)

Decapod larvae

Hemigrapsis sanguinea (Gifford & O’Connor, unpubl.)Cancer magister (Sulkin et al. 1998)

Miscellaneous crustaceans

Balanus cf. Crenatus nauplii (Turner et al. 2001)Freshwater cladocera (Wickham & Gilbert 1991; Pace & Vaque 1994; Wiakowsji et a. 1994; Adrian & Schneider-Olt 1999)

Bivalves

Crassostrea gigas (Dupuy et al. 1999)

Gelatinous zooplankton

Aurelia aurita (Stoecker et al. 1987)Mnemiopsis leidyi (Stoecker et al. 1987; Sullivan & Gifford, submitted)

Larval fish

Theragra chalcogramma (Lessard et al. 1996; Nishiyama & Hirano 1985)Gadus morhua (Von Herbing & Gallager 2000))

Chl a

Globec 01: Patterns of Energy Flow and Utilization on Georges Bank

Funding: National Science Foundation: $1,500,000Timeline: 2001-2005

Principal Investigator: Dian Gifford, University of Rhode IslandCo-Investigators: James Bisagni, University of Massachusetts

Jeremy Collie, University of Rhode Island Edward Durbin, University of Rhode island

Michael Fogarty, NMFS, Woods Hole Jason Link, NMFS, Woods Hole Lawrence Madin, Woods Hole Oceanographic Institution David Mountain, NMFS, Woods Hole Debra Palka, NMFS, Woods Hole

Michael Sieracki, Bigelow Laboratory for Ocean Science John Steele, Woods Hole Oceanographic Institution Barbara Sullivan, University of Rhode island

General Objective: To provide a broad ecosystem context for interpretation of the population dynamics of Georges Bank GLOBEC target species.

Specific Objectives:

Examine alternate model outcomes of GLOBEC and GLOBEC-related studies

Examine the mechanisms forcing changing patterns of energy flow on Georges Bank

With explicit consideration of factors not addressed in earlier models of the system:

Sources and fates of new production The role of the microbial food web in production processes Secondary production processes, including the apparent secondary production deficit Changes in invertebrate and vertebrate predator species composition in the context of population dynamics of GLOBEC target organisms Effects of environmental forcing on production processes during contrasting (~decadal) time periods

Scientific approach:

(1) Combine top-down [consumption-based models] and bottom-up [production-based models] approaches to describe Georges Bank food web

(2) Use these analyses as a precursor to dynamic modeling

Principal tools:

Linear network analysis (Vezina, 1999; 2000)

Nonlinear dynamical modeling (Collie and Delong 1999).

Focus on two major issues:

(1) Imbalance between primary production and fish production. “leakage hypothesis” v. microbial web dynamics

(2) Magnitude of top-down [fish] v. bottom-up [microbial web] processes

Locations of three spatial domains on Georges Bank derived from anEOF mode 1 SST map (Bisagani et al. 2000). GBC=Georges Bank Crest. TMF = Tidal Mixing Front. GBSF = Georges Bank Southern Flank. Spatial domains change with season.

1 9 6 0 1 9 6 5 1 9 7 0 1 9 7 5 1 9 8 0 1 9 8 5 1 9 9 0 1 9 9 5 2 0 0 0

Y e a r

-2

-1

0

1

2

19 75 19 80 19 85 19 90 19 95 20 00

Y ear

- 1.5

- 1.0

- 0.5

0.0

0.5

1.0

A

B

A. Spring (open bars) and fall (filled bars) bottom temperature anomalies for Georges Bank. The data are from NMFS spring (1968-2000) and fall (1963-2000) trawl surveys. The anomalies are referenced to the MARMAP data set (1977-1987).

B. Spring (open bars) and fall (filled bars) salinity anomalies for Georges Bank. The data are from NMFS spring (1968-2000) and fall (1963-2000) trawl surveys. The anomalies are referenced to the MARMAP data set (1977-1987).

Temperature

Salinity

Gadoids

0

200

400

600

800

1000

1200

1964 1969 1974 1979 1984 1989

Year

Observed

Multispecies model

Yield

Flatfish

0

10

20

30

40

50

60

70

80

1964 1969 1974 1979 1984 1989

Year

Elasmobranchs

0

50

100

150

200

250

1964 1969 1974 1979 1984 1989

Year

Pelagics

0

100

200

300

400

500

600

700

1964 1969 1974 1979 1984 1989

Year

Changes in fish abundances on Georges Bank since the 1960s (Collie and Delong, 1999):

Decreasing gadoids and flatfish Increasing pelagics and elasmobranchs

Temporal Stanzas: three time periods are defined on the basis of the historicaltemperature record:

Seasons: three seasons are defined on the basis of mixing regime: September-April: well-mixedApril-June: episodic stratificationJune-September: stratified

Stanza Physical Regime Fishery

regime

Fish Community

Structure

Data

1960s-early1970s

Cold watertemperature

High catchesby distant-water fleets

Abundantgroundfish

CPR,NMFS,Literature

1985-1995 Average watertemperature

Overfishing ofprincipalgroundfish

Peak inelasmobranchs &pelagicsGroundfish atlowest levels

MARMAP,GLOBEC,NMFS,Literature

1995-present Warm watertemperatureLow salinity

F ishingmortalityreduced

GroundfishrebuildElasmobranchs &pelagics peak

GLOBEC,NMFS,Literature

Pre-RecruitFish

DemersalFish

PelagicFish

Pelagic Microbial Food Web

VertebratePredators

Small InvertPredators

Meso-Zooplankton

(>200 um)

BenthicFood WebMacro-

Benthos

Meio-Benthos

Nano- and Micro--Phytoplankton

Nano--Zooplankton

(<20 um)

Micro-Zooplankton(20-200 um)

Bacteria

Detritus

NO3

Physics+

Climate

ElasmobranchFish

Birds & Mammals

Pelagic Metazoan Food Web

Large InvertPredators

Invertebrate Predators

PROJECT MANAGEMENT

Investigator Responsibility

D. Gifford Project coordination. Microbial web component:microzooplankton distribution, abundance, biomass,transfer rates

J . Bisagni Primary (new) production. Physical oceanography.

J . Collie Dynamical modeling. Benthos component:distribution, abundance, biomass, transfer rates

E. Durbin Secondary production (mesozooplankton) component:distribution, abundance, biomass, transfer rates

M. Fogarty Dynamical and energy flow modeling. Fisherieshistory of Georges Bank

J . Link Benthic and pelagic fish components: distribution,abundance, biomass, transfer rates

L. Madin Invertebrate predator component (large): distribution,abundance, biomass, transfer rates

D. Mountain Climatic history of Georges Bank. Physicaloceanography.

D. Palka Marine bird and mammal component: distribution,abundance, biomass, transfer rates

M. Sieracki Microbial web component: nanoplankton distribution,abundance, biomass, transfer rates

J . Steele Inverse and energy flow modeling. Science guru.

B. Sullivan Invertebrate predator component (small): distribution,abundance, biomass, transfer rates

Documents

Why do biological oceanographers care about planktonic protozoa (i.e., microzooplankton)?