Zooplankton Ecology in
Oceanic Oxygen Minimum Zones:
Structure, Trophic Webs, and Global Change
Karen Wishner University of Rhode Island
Liege 2014
OMZ
Future
Expanded OMZ
Boundary Effects
Boundary Effects
Eastern Tropical Pacific (ETP):
A distinct zooplankton biogeographical habitat
• ETP endemics
• Or, warm water distribution with ETP hiatus
Hypothesis
Species that vertically migrate must be adapted to the sharp gradients and extreme environments of the ETP
(low oxygen, abrupt thermocline)
Euphausiid species
Brinton maps in Reid et al.
SIO zooplankton and physical
oceanography group (McGowan, Brinton,
Fleminger, Reid) (1960’s-1970’s)
Some key technological advances for
analyzing vertical distributions in OMZs
Day Night
ADCP record of acoustic backscatter
JGOFS Arabian Sea
Data of C. Flagg in Morrison et al. 1999
JGOFS Arabian Sea (1990’s)
Widespread use of electronic oxygen sensors on zooplankton nets
Acoustics and OMZs: Extensive layers, diel vertical migration into OMZs
ROVs in OMZs: gelatinous fauna (MBARI)
Robison 2009
“Double MOCNESS” used in JGOFS
Sampling
90°W 100°W
10°N
20°N
Costa Rica Dome
Tehuantepec Bowl
MOCNESS Tows
0-1000 (1200) m Day and Night
Vertically stratified
8 – 24 strata per profile
Eastern Tropical Pacific Project
Oxygen at 500 m (NODC website)
JGOFS Arabian Sea Volcano 7
2007 Sta. 1
Mixed Layer
Upper Oxycline
OMZ Core
Lower Oxycline
Suboxycline
Fluorescence
OMZ Ecological Zones
Zones are unique
ecological habitats
• zooplankton
• oxygen
• predators
• food
Variable depths
Wishner et al. 2008, 2013
1.8 µM, 0.04 ml/L
9 µM, 0.2 ml/L
Oxygen Environment
Levin et al. in press
Spatial and temporal oxygen
variability at many scales
Many animals in OMZ
regions experience more
variability in oxygen and
temperature in their daily
lives from vertical migration
than they might experience
longterm.
Stramma et al. 2008
3 Themes and 3 Questions about OMZ Zooplankton
• BIOMASS AND DISTRIBUTION
• FOOD WEBS
• PHYSIOLOGY
“Normal” Zooplankton Biomass Distribution Not in OMZ Regions
Steinberg et al. 2008. VERTIGO project
Subtropical
Subarctic
OMZ Zooplankton Biomass Distribution Zonation, Boundary Layers, Thresholds
Narrow biomass peaks within Upper and Lower Oxyclines, “hole” in OMZ Core Diel vertical migration into OMZ Core and Upper Oxycline
KN08 St 8 Day
0306090120
1000
800
600
400
200
0
De
pth
mg/m3
200 um
500 um
1000 um
2000 um
5000 um
120 60 0
KN08 St 8 Night
0 30 60 90 120
1000
800
600
400
200
0
De
pth
mg/m3
5000 um
2000 um
1000 um
500 um
200 um
60 120
0.1
0
500
10 1000
mg/m3
mg/m3 mg/m3
Day Night 2008
Costa Rica Dome
Night
Day
> 5 mm
2 - 5
1 - 2
0.5 - 1
0.2 - 0.5
0
200
400
600
800
1000
De
pth
(m
)
DVM layer
Lower Oxycline layer
Thermocline layer
LO
OMZ Core DVM
Log biomass
2 µM
(0.045 ml/L)
Wishner et al. 2013
OMZ Pelagic Zonation: ETP
Day
Mixed Layer
Night
Upper Oxycline-A
Upper Oxycline-B
0 m
20
150
350 m
Day Night
OMZ Core
Lower Oxycline
Suboxycline 1200 m
750
550
350 m
Epipelagic OMZ Core--Day
Lower Oxycline
0 0.2 0.4 200
1000
800
600
400
Oxygen (mL/L)
Dep
th (
m)
OMZ Pelagic Zonation: Arabian Sea
OMZ
E. inermis Euchaeta spp.
Gaetanus spp. Haloptilus spp.
H. longicornis L. hulsemannae P. johnsoni
S. subtenuis Amphipods
Euphausiids Shrimp Ostracods
Chaetognaths Polychaetes Myctophids Cyclothone spp.
R. rostrifrons Megacalanidae
Photos: R. Williams
Congeners
1 0 2 3
(#/m3)
L. ovalis (#/ 10 m3)
L. hulsemannae
L. flavicornis
Lucicutia clausi
Boundary Species (#/m3)
0
400
1200
0 20 40
800
Night Day
Metridia brevicauda
0 5 0 10 15
Heterostylites
longicornis
LO Species (#/m3)
Boundary Effects: Copepod Distributions
• Distribution peaks associated with depth, oxygen, and OMZ boundaries
Wishner et al. 2013
Diel vertical migration (DVM) into lowest oxygen
water, mostly by larger taxa
Mixed Layer
Upper Oxycline A
Upper Oxycline B
OMZ Core
Lower Oxycline
Suboxycline
Day Night Night Day
> 5 mm
2 - 5 mm
1 - 2 mm
0.5 - 1 mm
0.2 - 0.5 mm
Biomass size class
proportions by zone
DVM: Species Distributions (ETP)
• Daytime layers in Upper Oxycline and OMZ Core
• Daytime depth and oxygen vary by taxon
• Most extensive DVM done by larger taxa
OMZ
0
300
600
De
pth
(m)
(#/m3)
Pleuromamma
abdominalis abyssalis
0 10 20 30
150
450
(#/m3)
Pleuromamma gracilis
0 6
Day
Night
12
(#/m3)
Euphausiid Gr 1
0 1 2 0.08
(#/m3)
Myctophid > 22 mm
0 0.04
OMZ Core
Wishner et al. 2013
Lower Oxycline Community Distinct multispecies assemblage
Shrimp
0
400
1200
800
5 0 10 15
Heterostylites
longicornis
(#/m3)
De
pth
(m
)
1 0 2 3
Lucicutia
hulsemannae
(#/m3) 0.04 0 0.08
Pleuromamma
johnsoni
(#/m3) 0.04 0 0.08
Cyclothone
spp.
(#/m3)
(#/ 100 m3)
Gennadas
spp.
0.5 0 1
3 Copepod Species
Fish
OMZ Core
Wishner et al. 2013
Lower Oxycline and Life History Strategy Arabian Sea copepod
F
C4
MWD
Wishner et al. 2000. Living in suboxia: ecology of
an Arabian Sea oxygen minimum zone copepod.
Limnol.Oceanogr. 45:1576-1593.
1000 0 0.2
Oxygen (mL/L)
0
Abundance (#/1000 m3)
C3
C2
C5
M
Depth
(m
)
Vertical Distribution 0
400
600
800
1000
400
600
800
1000 Me
an
We
igh
ted
De
pth
(m
)
C3
C4 C2
C5
F
M Adults F
C4
600
800
1000
De
pth
(m)
#/m3 Eucalanus
0
1 2
50 25 75
1
#/m3 LO fish, shrimp 0
400
Eucalanus inermis
Lower Oxycline Eucalanus
Lower Oxycline
Lower Oxycline and Life History Strategy Eastern Tropical Pacific copepod
Wishner et al. 2013
Oxygen Minimum Zone Core
Lower
Oxycline
Community
Eucalanus Layer at
Lower Oxycline
Monsoonal Life History Strategy Arabian Sea copepod Calanoides carinatus
Smith 2001
Spatial Comparison: a proxy for temporal change
Hydrography
Oxygen (µM)
0 0 20 20 40 40
De
pth
(m
)
0
0
500
500
1000
1000
2007
2008
Temperature (°C)
0 0 10 10 20 20 30 30
TB CRD
UO
OM
LO
SO
UO
OM
LO
SO
ML
ML
UO
OM
LO
SO
UO
OM
LO
ML
ML
90°W 100°W
10°N
20°N
Costa Rica Dome
Tehuantepec Bowl
OMZ Spatial Comparison: Biomass Layers
Costa Rica Dome KN08 St 8 Night
0 30 60 90 120
1000
800
600
400
200
0
De
pth
mg/m3
KN08 St 8 Day
0306090120
1000
800
600
400
200
0
De
pth
mg/m3
0.1 1 10 100 1000
500
0
mg/m3
120 60 0 60 120
1000
mg/m3
KN08 St 1 Day
020406080100120
1000
800
600
400
200
0
Dep
th
mg/m3
Kn08 St 1 Night
0 20 40 60 80 100 120
1000
800
600
400
200
0
Dep
th
mg/m3
Tehuantepec Bowl Day Night
mg/m3 mg/m3
0.1 1 10 100 1000
500
0
120 60 0 60 120
1000
OMZ
> 5 mm
2 - 5
1 - 2
0.5 - 1
0.2 - 0.5
Night
Day
Size Fractions DVM
DVM
LO
LO
DVM
LO
DVM
LO
0
0
1000
1000
Depth (m)
Wishner et al. 2013
Dep
th (
m)
0 60 120
10 Nov 07
CRD
M, C5M, Imm
F
0 60 120
29 Dec 08
CRD
F, M, Imm
F, C5M
F
0
400
800
0 60 120
OMZ
28 Oct 07
TB
Imm, C3, F, M
0 60 120
205
19 Dec 08
TB
C1, C2, Imm
Imm, C5M, F
Abundance (#/m3)
Life History Strategy and OMZ Variability Eastern Tropical Pacific copepod Eucalanus inermis
Wishner et al. 2013
OMZ
Now Future
Expanded OMZ
Now Future
OMZ Expansion Scenario
Lower Oxycline
DVM DVM
Lower Oxycline Constant oxygen
Deeper, colder
Constant depth
More time at lowest oxygen
Wishner et al. 2013. Zooplankton in the Eastern
Tropical North Pacific: Boundary effects of
oxygen minimum zone expansion. DSR I 79:122-
140.
Figure based on Seibel 2011
OMZ Zooplankton Trophic Webs
Zooplankton Feeding in OMZs: OMZ zooplankton are
omnivorous, with even a single copepod species feeding at
multiple trophic levels
• Surface Flux
diatoms, picoautotrophs
• Deep-Sea Detritus
“olive green material”,
amorphous material
• Zooplankton Remains
cuticle, nematocysts
• Deep-Sea Aggregates
bacterial clusters
Gut Contents include:
TEMs of gut contents: M. Gowing
Algal cell
Bacterial Aggregates
Cyanobact. Virus
Gowing and Wishner 1992, 1998
Food Sources: Stable Isotope Approach
• δ13C of zooplankton is similar to initial POM carbon source
0.1-1‰ increase per trophic level
• δ15N of zooplankton increases with each trophic level
1.5-4‰ increase per trophic level
Indirect indicator of some nitrogen cycle processes
Basic assumption: Zooplankton eat POM (1 trophic step)
Measured stable isotopes of zooplankton and POM during ETP Project
Vertical profiles at 2 stations (TB, CRD) in 2 years
Size-fractionated zooplankton (mixed assemblage) from MOCNESS tows
POM from pumps (Wakeham)
PhD of Rebecca Williams, URI, 2013
δ15N Vertical Profiles
2007 2008
TB CRD TB CRD
POM Zooplankton Williams et al. in press DSR
O
OMZ
POM as a Food Source
Tehuantepec Bowl Costa Rica Dome
Shallow (0-110m)
Deep (110-1000m)
POM as a Food Source: Consumer Polygons
Tehuantepec Bowl Costa Rica Dome
Shallow
Deep
Deep
Shallow
Williams et al. in press
Polygons: POM values with 1 trophic level increase
Potential values for zooplankton consuming POM
Deep
Shallow
ML
UO
OM
LO
LO- E. inermis
Zooplankton as POM Consumers
Tehuantepec Bowl Costa Rica Dome
Williams et al. in press
ML
UO
OM
LO
LO- E. inermis
Previous ETNP
(denitrification)
Zooplankton Trophic Webs & Denitrification
Tehuantepec Bowl Costa Rica Dome
Williams et al. in press
Zooplankton Trophic Webs
Sources of Low δ15N
Tehuantepec Bowl Costa Rica Dome
N2 Fixation
& Upwelling
ML
UO
OM
LO
LO- E. inermis
Williams et al. in press
Pelagic Trophic Effect
at Lower Oxycline
Wishner et al. 2013
1000
Dep
th
(m)
0 5 10 15
TR
0 5 10 15
T
R
Zooplankton δ15N (%o)
0
1000
DVM
1000 0.1 10
Dep
th
(m)
0.1 10 1000
LO
LO
DVM
Zooplankton Biomass (mg/m3)
0
Temperature (°C)
Oxygen (µM)
0
10 20 30
20 40
Ox T
0
1000
10 20 D
ep
th
(m)
30
0 20 40
T Ox
Gradient in zooplankton δ15N at Lower Oxycline
Indicator of feeding up the trophic web
Associated with LO biomass layer
Shifts depth with oxygen
Implications for biogeochemical cycling
Midwater zone of activity shifts depth
TR
Lower Oxycline: Benthic-Pelagic Coupling Volcano 7 Seamount
800 m
730 m
Lower Oxycline T, O2 and zooplankton layer oscillate with tidal cycle
Impacts food availability for benthos
0
1
2
3
Lowest O2
Tem
per
atu
re
Dep
th (
km)
TIme
Wishner et al. 1990, 1995
Levin et al. 1991, Levin 2002
OMZ Zooplankton Physiology
OMZ Metabolism
Animals can regulate their metabolism at oxygen levels
down to minimum [O2] in environment
• Increased aerobic efficiency
• Anaerobic pathways
• Behavior: DVM up to higher oxygen habitat to repay oxygen debt
• Metabolic suppression
Seibel 2011. Critical oxygen levels and metabolic suppression in
oceanic oxygen minimum zones. J. Exp. Biol. 214:326-336.
Total Metabolic Rate Aerobic plus anaerobic energy equivalents
ATP turnover
Anaerobic
Glycolysis
Aerobic
Oxidative
phosphorylation
Cytosol
Mitochondria
Lactate/
Octopine
NAD+ NADH
Glucose Pyruvate
ADP ATP
Kreb’s
Cycle
NADH
NAD+
CO2
NAD+ NADH
O2 H2O
e-
• Molecular markers of
reduced protein synthesis
• Chemical products of
anaerobic metabolism
Seibel slide
0
20
40
60
80
100Lactate ATPMO2 ATP
To
tal M
eta
bolic R
ate
(A
TP
g-1
h-1
)
E. eximia N. gracilis E. diomedeae
21 0.8 21 0.8 21 1.6
Seibel 2011, in prep
Total metabolic rate = sum of aerobic (gray) and anaerobic (black) processes
Metabolic suppression at daytime depth in OMZ compared to nighttime depth in
oxygenated water near surface (after accounting for T)
Must ascend to oxygenated water to repay oxygen debt
Affects carbon budgets for estimates of active carbon export (respiratory CO2)
Metabolic suppression in OMZ of 30 – 60%, many taxa
3 ETP euphausiid species, diel vertical migrators
Metabolic Suppression in the OMZ
Creseis
virgula
Hyalocylis striata
Diacria
quadridentata
Cavolinia longirostris
Clio
pyramidata
Maas et al., 2012a, b.
Multiple Stressors and
OMZ Pteropod Metabolism
High T: all species increased
metabolism
Low O2: migrators had
metabolic suppression,
repay O2 debt at surface but
higher T may interfere
High CO2: only non-migrator
decreased metabolism
Species %
of
con
trol
T O2
CO2
3 Interesting Questions
about OMZ Zooplankton
Question 1
Habitat Compression, Zooplankton, and Fish
With OMZ expansion, how will shoaling of the upper oxycline and
its zooplankton layers affect fish populations and fisheries?
Will this change prey availability, composition, nutritional value, or
accessibility to fish seasonally or geographically?
Question 2
Trophic Connection between OMZ Microbes
and Zooplankton
Are OMZ microbial processes and metazoan food webs
connected via an OMZ-specific microbial loop?
Or a gelatinous food web?
Does OMZ microbial production enter zooplankton food webs?
Question 3
OMZ Zooplankton and Export Flux
Does reduced OMZ zooplankton biomass, vertical redistribution
of species and biomass, and metabolic suppression affect
export flux and biogeochemical cycling in OMZ regions?
“Martin curve” C flux NE Pacific (Martin et al. 1987) LO zpl layer: eat, repackage
New particles (fecal pellets) produced?
OMZ: Sparse zpl, metabolic suppression
Particles sink fast, not eaten or broken up?
More? or less? carbon sequestration
Qualitative or quantitative difference from non-OMZ?
Conclusions
The unique characteristics of OMZ zooplankton
distributions, trophic webs, and physiology affect
ecological function and ecosystem dynamics.
Zooplankton layers at the upper and lower oxyclines will
shift depth with OMZ expansion, potentially impacting
food webs, fisheries, and biogeochemical cycles.
Main Collaborators
Daly, Gowing, Levin, Roman, Seibel, Smith, Wakeham
Students Ashjian, Cass, Elder, Maas, Rapien, Saltzman, Williams
Technicians Gelfman, Outram, Schoenherr
Many other colleagues, technicians, postdocs, students, crew
Funding
– National Science Foundation
-- University of Rhode Island
Future Research Directions:
OMZ Zooplankton and Global Change
• Finer scale and longer term spatial, vertical, and temporal sampling that
directly connects zooplankton with environmental parameters including
their predators and prey
• OMZ microbial loop and gelatinous food web studies
• Understanding of OMZ microbes, particles, and aggregates in situ
• New technology (sensors, environmental “– omics”) and in situ methods
for studying zooplankton distributions, physiology, and export flux
• Modeling that accounts for shifting zooplankton oxycline boundary layers
and metabolic suppression
• Impact of multiple stressors
δ13C Vertical Profiles 2007 2008
TB CRD TB CRD
POM Zooplankton
30 min
Humboldt Squid
Critical Oxygen Partial Pressures Metabolic suppression below Pcrit
4 hours
12 hours 12 hours
Wishner et al. 2008
OMZ Zones Differ in Community Structure Arabian Sea copepods
Species Diversity Rank Order of Abundance
A possible reproductive response by an LO copepod to seasonal particle and carbon fluxes (Arabian Sea)
C2 Adult
Jan Mar Sept Dec
C2
C3
C4
C5
M
F
SW
Monsoon NE
Monsoon Wind
Flux
Honjo et al. (1999)
Pro
port
ion
0.4
0.2
Young stages
appear a few
months after flux
event
Wishner et al. 2000
Copepod Zonation
through the OMZ and Lower Oxycline (Arabian Sea)
Mean Weighted Depth (center of distribution) and
mean Oxygen at that depth for each species
Each point is a different species Point types represent different Species Groups
300
400
500
600
700
800
900
1000
0.00 0.02 0.04 0.06 0.08 0.10 0.12 0.14
Oxygen (ml/L)
Me
an W
eig
hte
d D
ep
th (
m)
SG 1 SG 2
SG 3 SG 4
SG 5
SG 6
SG 7
SG 8
SG 9
Wishner et al. 2008
