4/17/23

Marine food web interactions What is in the water?

Viruses, bacteria (heterotrophic, chemosynthetic),
phytoplankton, zooplankton (micro, meso, macro; holo-,
meroplankton), nekton, benthos

Monika Winder
monika.winder@su.se
Stockholm University

Whale Shark (Rhincodon typus)

Source: Wikimedia Commons

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We can not (or should not) separate biology from Pathways of carbon flow in the pelagic systems
the environment

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Species interactions
Who interacts with whom?
• Trophic (feeding) interactions
• None-feeding interactions: Symbiosis
two or more species living purposefully in direct
contact
– Mutualisms: all individuals benefit from the
relation (obligate or facultative)
– Parasitism: the parasite benefits from another
individual, while harming the host
Source: havet.nu

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Species interactions Pelagic food web is unique

• Trophic interactions • Size structured: big organisms eat smaller
• Non-feeding interactions: symbiotic, parasitic organisms – predators are larger than their prey

Source: Kira Askaroff

Vargas et al. (2015) Science.

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Trophic level in agricultural and aquatic food chain

Pelagic food web is unique
• Size structured: big organisms eat smaller
organisms – predators are larger than their prey
• Majority of biological activity (>90%) takes place
in microorganisms, which includes organisms
feeding on at least 4 different trophic levels
(terrestrial ecosystems: carnivores eating other
carnivores or trophic level 4 are not common)

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What regulates population Marine primary production

dynamics from phytoplankton
to fish?

The key to answering ecological

questions lies in understanding the
energy flow in the ecosystem

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Which Energy Flows in Marine Ecosystems? Who is

Marine primary production controlling Whom?

• Oceanic phytoplankton fix 40-50 Gtons C yr-1

• terrestrial systems fix 50-65 Gt C yr-1
• standing stock of phytoplankton 0.30-0.75 Gt
C, with a turnover time of 2-6 d (!)
• terrestrial standing stock 800 Gt C, with a 13-
16 yr turnovertime
• regulator of global climate, both evolutionarily,
climatically

Bottom-Up Top- Down Wasp-Waist

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The Very Small drive the Very Large The classic view:
Food chain
Secondary consumers
Trophic level 3
Fish

Primary consumers CO2

Trophic level 2 Nutrients

Zooplankton

Primary producers
Trophic level 1
Phytoplankton

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Matter vs. Energy Ecological efficiency

= Amount of energy passed from one link to the next
Energy and carbon content of organic matter are tightly Example: Ecological Efficiency 10 %
correlated
Production (P3) 2.5
BUT Fish (1% of P1)

Matter: is recycled (at least partially) Energy loss

(~90 %)
Production (P2) 25
Energy: no recycling, unidirectional flow (10% of P1)
• 2nd law of thermodynamics (heat loss at energy transfer)
Copepod
à energy is lost between trophic level
Energy loss
• Refractory organic matter is not converted into energy (~90 %)
Production (P1) 250
• Energy invested differently than in organic matter (e.g., 100 %
locomotion) cannot be used by higher trophic level g C m-2 y-1
Phytoplankton

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… but the world is more complicated:

Ecological efficiency
= Amount of energy passed from one link to the next
Food web

TL = 3-4
à Most of the energy (sun light) Animals feed at different Fish
Fish

Energy loss
fixed by phytoplankton gets lost trophic levels à
(~90 %) à A large number of links lead to number of step varies TL = 2-3 CO2
Nutrients
more efficiency losses
Copepod à The number of possible trophic TL = 2
Zooplankton

Energy loss levels is limited

(~90 %) Ciliates

Phytoplankton
Phytoplankton

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… the world is even more complicated: … the world is even more complicated:
Microbial Loop Microbial Loop
“Loop” – recycling
TL = 4-5
CO2 and nutrients release à Fish à increase in trophic steps Fish

re-used by phytoplankton à low available energy for

DOC excretion à
CO2
upper trophic levels TL = 3-4 CO2
used by bacteria Nutrients Nutrients

Zooplankton Zooplankton

Ciliates Ciliates
HNF HNF

Bacteria Bacteria
Phytoplankton Phytoplankton
DOC DOC

HNF: heterotrophic nanoflagellates HNF: heterotrophic nanoflagellates

DOC: dissolved organic carbon DOC: dissolved organic carbon

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Nutrient availability affects phytoplankton cell size

Size matters! and species interactions

Implications of size-structured food web: TL = 2 TL = 3-4 TL = 4-5

Trophic level

• Size of phytoplankton cells influences trophic Cil

structure and number of possible trophic levels
HNF

HB
What controls phytoplankton cell size?
• Nutrient availability (bottom-up)
Size (micrometer) Size (micrometer)
• Grazing (top-down) Diatoms Pico- and nanoplankton Large-sized algae
• Turbulence high nutrients (small algae) (Cyanobacteria)
high Si:N low nutrients eutrophication
Phytoplankton dominance
Source: Kira HNF: heterotrophic nanoflagellates
Askaroff HB: heterotrophic bacteria Modified after Sommer et al. (2002)
Cil: Ciliates

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Nutrient availability affects phytoplankton cell size Nutrient availability affects phytoplankton cell size
and species interactions and species interactions
TL = 2 TL = 3-4 TL = 4-5 TL = 2 TL = 3-4 TL = 4-5
Trophic level

Trophic level
Size (micrometer) Size (micrometer)
Diatoms Pico- and nanoplankton Large-sized algae Diatoms Pico- and nanoplankton Large-sized algae
high nutrients (small algae) (Cyanobacteria) high nutrients (small algae) (Cyanobacteria)
high Si:N low nutrients eutrophication high Si:N low nutrients eutrophication
Phytoplankton dominance Phytoplankton dominance

Modified after Sommer et al. (2002) Modified after Sommer et al. (2002)

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Bottom-up Control Parallel long-

westerly weather

term trends
• Under bottom-up control, the physical environment
drastically affects the overall productivity of across four phytoplankton zooplankton
ecosystems and the dynamics of fish assemblages. trophic levels
• Decadal-scale regime shifts suggest the existence of and
multiple stable states in fish communities. weather Herring Kittiwake laydate

in the North Sea

• A Bottom-up control offers a comprehensive
framework for understanding how different
components would react to environmental changes (Aebischer et al. 1990, Nature) Kittiwake clutch Kittiwake chicks
or to changes at the bottom of the food chain.

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What makes the largest pelagic animals (baleen whales,

whale sharks) so special and the most abundant fishes The food chain from primary producers to fish
(anchovies, herrings) so successful? is longer in nutrient-poor systems compared to
upwelling regions with high nutrient and silica –
is this correct?
1) They are very efficient predators.
1) Yes, because in nutrient-poor systems small
1) They eat plankton and have a lot of food available phytoplankton dominate and most of the energy is
transferred through the microbial food web.
by eliminating many intermediate trophic steps.
2) No, because diatoms dominate, which are grazed by
copepods and these in turn by fish.

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Which Energy Flows in Marine Ecosystems? Who is

controlling Whom? Top-Down Control

Bottom-Up Top- Down Wasp-Waist

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The Very Large drive the Very Small

Bigger Fish
Eat
Smaller Fish

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Predators are
constrained by the size
of their jaw and prey
Top-Down Control
fish that are less than
1/3 their own size • A top-down control can help to understand several
observed ecological patterns at an ecosystem level
when removing top predators.
Who is eating whom?
Cannibalism, omnivory

• Not all cascades propagate to lower trophic levels

or have significant impacts on ecosystem processes
as numerous compensatory mechanisms dampen
Size-based predation provides an or eliminate them.
explanation for observed
abundance patterns in marine
ecosystems

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Which Energy Flows in Marine Ecosystems? Who is

controlling Whom?
Wasp-Waist Control

or

the role of dominant forage fish species

Bottom-Up Top- Down Wasp-Waist

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Small Pelagic Fish (or Forage Fish) Small Pelagic Fish

• abundant and central in the ocean food-webs,
• relatively few species (300-400),
• feed on plankton,
• form large schools to compensate their size,
• experience rapid population expansion because of their
relatively small size, fast growth, early maturity, and relatively
high fecundity,
• their short life span can also lead to sudden population collapse
when adult mortality rates are high or recruitment is low

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Small pelagic fishes drive both the very large and the very small:
Small Pelagic Fish as predator the energy flow is controlled up and down from the middle.

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37% catches
Small Pelagic Fish fisheries 15% sales value

Catches and landing values by groups of species. Source: World Ocean Review 2010.

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Fishing down the food-web Wasp-Waist Control

• One or few forage species support a high diversity of
larger predators.

• Under wasp-waist control, the collapse of a dominant

prey species can generate drastic changes at higher and,
more surprisingly, at lower trophic levels.

• As fisheries remove substantial amounts of small pelagic

fish one must carefully consider the implications for the
other species in the ecosystem.

Source: Sea around us project.

• The assumption of wasp-waist control has not been
empirically tested in all ecosystems.

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Proposed generalisations for ecosystem structure:

• Control by the environment (bottom-up control)
predominates.
California Canary
current current Kuroshio
• Control by predators (top-down control) plays a current
role in dampening ecosystem-level fluctuations.
Benguela
• Trophic cascades are seldom found, except in lakes, current
Humboldt
or in marine hard substrata ecosystems and mainly current
for less complex food-webs.

• Wasp-waist control is most probable in upwelling

systems.
The most productive areas in the world's oceans
(Bakun, 1996; Cury et al., 2000).

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Baltic Sea food-web

Case studies from the Baltic Sea

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Baltic Sea food-web

Cod body condition
1980s c. 2016

à Eutrophication

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Cod body condition

Effects of fishing on fish populations Low condition à increased mortality
and/or decreased growth à ⇊ large cod
individuals

Casini M et al. 2016 Hypoxic areas, density-dependence and food limitation drive the body condition of a heavily exploited marine fish
predator. R. Soc. open sci. 3: 160416.

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Another important question:

Are seals exercising a top-down control in the
pelagic ecosystem of the Baltic Sea?

35000
Estimated number of grey

30000
25000
20000
seals

15000
10000
5000
0
1975 1985 1995 2005 2015

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Seals vs. Fisheries

Grey seals abundances and Are seals exercising a top-down control in the pelagic
distribution
Grey seals Halichoerus grypus in the Baltic
ecosystem of the Baltic Sea?

Cod fishing mortality:

Co
d

Grey
seals

Salinity
Fcod1

MacKenzey et al 2011. PlosONE Fcod0.3

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Conclusions Methods for investigating species interactions

• Stable isotope data

• Fish biomass will be affected
primarily by fishing mortality rather • Diet DNA barcoding
than seal mortality
• Environmental metagenomic data combined
• Seal predation pressure on cod is with network modeling
highest under low fish biomass

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Tara Oceans studies plankton at Terminology

PLANETARY SCALE
• OUT Operational Taxonomic Unit
• Interactome: biological networks; species units
linked into a whole food web
• Node: species or taxa
• Edges: processes that move biomass from one group
to another (grazing, predation, parasitism)
• Motifs: sub-graphs that repeat themselves

http://www.embl.de/tara-oceans/start/

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• What was the goal of the study?

• How did the scientist approach this goal?
• What factors govern food web structure in general and
what did the study found were dominating factors?
• What type of biotic interactions did the study find? Give
some examples.
• Are species networks different among regions or was a
global pattern present?
• What type of species interactions were most abundant?
• What do you think is the most interesting finding of this
study?

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