Ecole Normale Supérieure - Licence de Biologie (L3) Ecologie & Evolution 2018-2019 « "Biodiversité, interaction et fonctionnement" »

Biodiversity, food-web architecture, and functioning of aquatic ecosystems in a context of anthropogenic perturbations Gérard LACROIX

UMR 7618 IEES-Paris – Institute of Ecology and Environmental Sciences of Paris, Université Pierre et Marie Curie, 7 quai St.-Bernard, 75005 Paris, FRANCE [email protected]

Biodiversity Biodiversity refers to the extent of genetic, taxonomic, and ecological diversity over all spatial and temporal scales (Harper & Hawksworth 1995, Phil. Trans. Royal Soc. Lond., B, 345: 5-12).

Functional or functioning By functional or functioning researchers mean the activities, processes, or properties of ecosystems that are influenced by its biota (production of biomass, nutrient recycling, …).

1

A sixth extinction crisis? Five mass extinctions : - Ordovician - Devonian - Permian - Trias - Cretaceous - Pleistocene Current extinction rates : 100 times higher than mean background “geological” rate Projected extinction rate : dramatic increase during this century

2

A strong increase of non-native species

3

Origin of the interest of scientists on Biodiversity an ecosystem functioning Occurrence of dramatic changes in distribution and abundance of biodiversity. Predicting the consequences of these changes on ecosystems or Earth-system functioning is a critical issue. This has only recently become a growing part of ecological research (ecology has been historically divided into two disciplines: community ecology and ecosystem ecology). Important conference in Bayreuth (Germany) in 1991 (Shulze & Money (eds)1994, Biodiversity and Ecosystem Function. Springer Verlag). 4

Number of papers (logarithmic scale) Publications (in logarithm scale) that included either “Ecology” (“ecological”), “biodiversity”, “ecosystem function(ing)”, or both since 1980 (Web of Science).

5

Human impact on environmental conditions

CO2 atmospheric concentration

Etheridge et al. Geophys Res, 101: 4115-4128 IGBP synthesis: Global Change and the Earth System (Steffen et al. 2004)

Atmospheric temperature

6

What are the major threats to aquatic ecosystems? Water   Pollu/on  

Over-­‐   Exploita/on  

Habitat   Degrada/on  

Flow     Modifica/on  

Species     Invasions  

The five major threat categories and their established or potential interactive impacts on freshwater biodiversity. Global changes (nitrogen deposition, warming, shifts in precipitation, runoff patterns) will  exacerbate   these  five  con/nuing  threats.  

From: Dudgeon, D., A. H. Arthington, M. O. Gessner, Z.-I. Kawabata, D. J. Knowler, C. Lévêque, R. J. Naiman, A.-H. Prieur-Richard, D. Soto, M. L. J. Stiassny & Caroline A. Sullivan (2006). Freshwater biodiversity: importance, threats, status and conservation challenges. 7 Biological Revue, 81: 163-182.

Why should we care?

8 From: Poff, N. L., M. M. Brinson & J. W. Day, Jr. (2002). Aquatic ecosystems & global climate change: Potential impacts on inland freshwater and coastal wetland ecosystems in the United States. Pew Center on Global Climate Change

Expected impact of climate change on lakes -  Global average surface temperatures on earth have increased by approximately 0.6°C over the last century -  Intergovernmental Panel on Climate Change (IPCC): increase in global average surface temperature of 1.4 to 5.8° C for 2100 -  Strongest temperature increases observed during late winter and early spring -  Expected changes in seasonal and inter-annual patterns of temperature, precipitations, wind (frequency of extreme events such as storms) and water residence time (lower in winter and higher in summer) -  Dominance of small and shallow lakes with weak buffering capacity against climatic events

For more details, see: Mooij et al. 2005. The impact of climate change on lakes in the Netherlands: a review. Aquatic ecology, 39: 381-400)

9

Expected effects of climate change on freshwaters - Climate change could alter the dynamics of the aquatic ecosystems -  rainfall and snowfall amounts -  Runoff and water levels -­‐  Dissolved  organic  C  and  water  transparency -  Ice cover (less ice cover could imply more water evaporation) -  Punctual water temperature changes might be very high - Stratification and dissolved oxygen (depth of mixing layer) -  Species composition (Nuisance algal species) - Thermal habitat for living species - Metabolism and decomposition rates - Ecosystem productivity

For more details, see: Mooij et al. 2005. The impact of climate change on lakes in the Netherlands: a review. Aquatic ecology, 39: 381-400)

10

Expected effects of climate change on freshwaters

Summer  condi/ons:   Warmer  epilimnion   (more  O2)   Cooler  hypolimnion   (less  O2)  

(From “Water on the web”

-­‐  Warmer  air  temperatures  reduce  volume  of  hypolimnion   -­‐  Produc/ve  lakes  have  less  Dissolved  oxygen  in  hypolimnion     -­‐  Large  cold-­‐water  fish  require  well-­‐oxygenated  hypolimnion   -­‐  Falling  lake  levels  reduce  extent  of  produc/ve  liNoral  zone  

11

Catchment processes and eutrophication - Eutrophication is an increase of nutrient (N, P) load in aquatic ecosystems leading to the increase of the production of planktonic primary producers production and (potentially toxic) cyanobacteria. - Eutrophication symptoms: -  Decrease of water clarity -  Large daily oscillations of O2, CO2, and pH shifts, -  Oxygen deficit (down to anoxia) in deep water layers -  Increase of internal nutrient loading -  Increase of cyanobacteria (potentially toxic strains) -  Decrease of water quality -  Fish kills, and general decrease of biodiversity -  Odour and aesthetic problems -  Lake death -  Expected effect of global changes: -  Increase of soil erosion due to more intense precipitation events (increase of dissolved organic carbon) -  Reduced flushing rates (longer inter-rains durations) -  warmer waters and more severe anoxia of hypolimnion waters (denitrification) ⇒ Probable increase of potentially toxic Cyanobacteria.

12

In a lot of lakes, phytoplankton primary production is naturally Phosphorus -limited

-  P-PO4-- rare in aquatic ecosystems -  Importance of bottom-up control (P-limitation) -  Lakes are mostly sinks of phosphorus (eutrophication = natural process) -  P increase => eutrophication -  Well oxygenated sediment: P complexed with Fe+++ and Al, etc. -  Anoxic sediment Fe++ => X 1000 P-release

Water P-load Spring total phosphorus (mg/m3)

From Dillon et Rigler (Limnology & Oceanography, 1974)

P-release from sediment

algal biomass Sediment anoxia

Increase of internal P-loading 13

Eutrophication and Leibig’s law -  Lake eutrophication primarily dependent upon: - Urban effluents - Agriculture fertilisation (65% N and 20% P water pollution) - Allochthonous inputs of organic matter with adsorbed nutrients (agriculture intensification, erosion, destruction of riparian areas)

-  Since 1950, importance of detergents (tripolyphosphates, TPP) -  Increase of P often changes limiting factor from P to N, and even to CO2

-  Low N/P ratio and N-limitation favour cyanobacteria: - often poorly controlled by grazers (trophic cul-de-sacs) - sometimes toxic for other algae, aquatic grazers, and mammals - Sometimes able of N2 fixation

N2 fixation needs nitrogenase enzymatic activity (from N2 to NH4+). Such fixation is made in anaerobic stage in specialized cells called heterocysts

14

Global warming and fish habitat in US streams Cool-­‐water  species:     +12%  with  a  2°C   constraint  

Warm-­‐water  species:  +  36°C  with  a  2°C   lower  range  constraint  

Cold-­‐water   species:    -­‐36%  

Almost  no  change  with  a  0°C   lower  range  constraint   -­‐15%  with  a  0°C  lower   temperature  constraint  

I with 2°C lower temperature constraint I with 0°C lower temperature constraint

Changes in fish suitable thermal habitats for US fishes (divided into 3 guilds according to thermal preferences) under the 2 × CO2 climate scenario. For cool and warm water fishes lower temperature constraints are set at 0 ◦C and 2◦C. Changes are given as percentages. (Adapted from Mohseni et al. [2003], Climatic Change, 59: 389-409).

15

Global warming and changes in fish communities

-  Species expected to migrate to maintain thermal preferences or tolerances - Higher latitudes or altitudes (but some alpine systems may be lost as headwaters retreats) - Migration requires connectivity of ecosystems. anthropogenic fragmentation (dams) may limit movements - Some cold-water species cannot cannot move northward or upward and will have no “refuge” during a period of regional warming.

16

Temporal processes and match-mismatch Peak first feeding of fish larvae

Match:

time Peak production of small zooplankton (rotifers, nauplii, etc.) Peak first feeding of fish larvae

Mismatch:

time Peak production of small zooplankton (rotifers, nauplii, etc.)

Different responses to temperature or responses to other factors (light, photoperiod) For more details, see: Mooij et al. 2005. The impact of climate change on lakes in the Netherlands: a review. Aquatic ecology, 39: 381-400)

17

Temporal mismatch

(a) Over 30 years, events associated with secondary consumers advanced less rapidly than those for both primary producers and primary consumers.

(b) Analysis of decadal phenological trends confirmed the difference in rates of change among trophic levels (less pronounced for secondary consumers).

(c) Over 30 years, no significant effect of environment on the decadal acceleration.

Asynchrony in rates of phenological changes in UK (Thackeray et al. 2010, Global Change Biology)

18

Potential effect of rising CO2 on transfer efficiency Daphnia: Tight stoichiometry

C:P

Seston: variable stoichiometry versus

-  Evidence for stoichiometric constraints on Daphnia growth

C:P

C

:P season

-  Rising CO2 levels with stagnant or decreasing P-load: 1.  Direct effects on phytoplankton growth and stoichiometry 2.  Indirect effects (input of allochthonous C from watershed) ⇒  Rising C:P levels of lake phytoplankton are likely ⇒  Expected decrease in transfer efficiency from phytoplankton to zooplankton

19 Elser et al. 1998, Ecosystems

Changes in body size

The tested hypotheses regarding the impact of warming on body size at different biological scales

Mean effect sizes (95% confidence intervals). SR = species richness. Ab. = abundances. M = marine. F = freshwater

Daufresne et al. 2009, PNAS

Ecological emergence of the Temperature Size Rule (TSR)

 

 

 

 

Ecology may play a major (dominant) role in the emergence of thermal (latitudinal) clines in body size Studies of the TSR should no longer ignore ecology in their designs The magnitude of warming-induced body downsizing depends on the strengths of competition and predation in the community In turn, warming-induced body downsizing is likely to alter ecological dynamics in predictable ways

Edeline et al. (2013) Global Change Biology, 19 (10): 3062-3068

20

Ecological emergence of the TSR

Warming shifts intraspecific competition from favoring larger sizes to favoring smaller sizes

Warming magnifies an always negative effect of inter-specific competition on body sizes

Warming reinforces a strongly negative effect of predation on body sizes Suggests that predators do not selectively target juvenile prey (that would select for increased prey size) 21

Effects of global changes on aquatic food webs Increased metabolic rates from warming should: -  increase competition for scarcer resources -  increase the sensitivity of specialist species and favor more connected food webs - reduce energy transfer efficiencies along food chains - favor the extinction of top predators - reduce vertical diversity in food webs - Favor extinctions and new invasions

X

-  change interaction networks

22

Reduction of top-predators and decrease in chain length Microorganism communities, with initially low or high diversity and 2 types of species (A and B), have been warmed in laboratory microcosms. Heated microcosms disproportionately lose top predators and herbivores, and become increasingly dominated by autotrophs and bacterivores.

23 Petchey et al. 1999, Nature

Invasions and extinctions in food webs (example of the Wadden sea food web)

24 Byrnes et al. 2007

Invasions and extinctions in food webs

25

The combination of multiple changes T = Temperature N = Nutrients Nutrient addition: No nutrient addition:

Effect of temperature (°C) on: (A)  ratio of heterotrophs to autotrophs (B)  Biomass of phytoplankton (C)  Biomass of microbes (D)  Biomass of zooplankton (E)  the entire food web. (Initial conditions indicated by horizontal lines).

O’Connor et al. 2009. PLOS Biology

26

Strong impacts of interaction webs on ecosystems (C) Long Lake (Michigan) with largemouth bass present (right) and removed (left). Bass indirectly reduce phytoplankton (thereby increasing water clarity) by limiting smaller zooplanktivorous fishes, thus causing zooplankton to increase and phytoplankton to decline. (D) Coral reef ecosystems unfished (right), and with an active reef fishery (left). Fishing alters predation and herbivory, leading to shifted benthic dynamics, with the competitive advantage of reef-building corals and coralline algae diminished in concert with removal of large fish. (E) Pools in Brier Creek, a prairie margin stream in south-central Oklahoma with (right) and lacking (left) largemouth and spotted bass. The predatory bass extirpate herbivorous minnows, promoting the growth of benthic algae (Estes et al. 2011).

27

Effects of anthropogenic perturbations on body size: Why is it so important ? Size-dependent functional food webs 28

Why is body size so important in aquatic systems? •  Role of body size in terrestrial systems explored extensively at very large spatial scales (e.g. latitudinal gradient) •  Prominent role in thinking about community structure in aquatic ecosystems: - Importance of particles and organisms in suspension in the water (also true for plants [planktonic algae] an detritus [detritic particles + algae = seston]) - Predation (including herbivory) frequently size-dependent in pelagic systems. In terrestrial systems, herbivory might be closer to parasitism. - Frequent use of body size when analysing aquatic organisms (flow, cytometry, coulter counter, continuous plankton recorder, remote sensing of fish with Passive Integrated Transponder [PIT])

See: Woodward G. & P. Warren (2007). Body size and predatory interactions in freshwaters: scaling from individuals to communities. In: Hildrew et al. (Eds): Body Size: the Structure and Function of Aquatic Ecosystems. Cambridge University Press, Cambridge: 98-117. 29

intra-specific variation in body size and particle selection by filter feeders Positive relationship between predator size and maximum bead size

Constant minimum bead size

Relationship between prey size and body size in the copepod Acartia tonsa capturing plastic beads (from Humphries [2007]. Body size and suspension feeding. In: Hildrew et al. (Eds): Body Size: the Structure and Function of Aquatic Ecosystems. Cambridge University Press, Cambridge: 98-117). 30

Maximal prey length (mm)

intra-specific variation in body size and particle selection by invertebrate raptors 1.4 1.2 1.0 0.8 0.6 0.4 0.2 0.0 3

4

5

6

7

8

9

10

11

12

Predator length (mm) Relationship between length of the carnivorous planktonic Cladocera Leptodora kindtii and the maximal body size of its prey (doted lines = 95% interval). (from Herzig & Auer.1990. Hydrobiologia 198: 107-117).

31

Largest particle ingested (diameter µm)

Body size of herbivorous Cladocerans (planktonic microcrustacea) and maximum size of filtered particles

Carapace length (mm) Relationship established for 7 species of Cladocerans (From Burns C. W., Limnology and Oceanography, 1968)

32

Feeding and size: processes at the individual level Prey = one Nemurella pictetii (Stone fly larva, Plecoptera) [head capsule width = 1 mm]

Handling time (s)

Log10 mg prey biomass consumed 24 h-1

Predator = Cordulegaster boltonii larvae (Odonata)

Log10 mg predator body-mass Handling time (i.e. for prey capture to complete ingestion) as a function of predator body mass.

Log10 mg predator body-mass Maximum daily consumption of N. pictetii as a function of predator body mass.

From Woodward G. & P. Warren (2007). Body size and predatory interactions in freshwaters: scaling from individuals to communities. In: Hildrew et al. (Eds): Body Size: the Structure and Function of Aquatic Ecosystems. Cambridge University Press, Cambridge: 98-117. 33

Biotic determinants of zooplankton body size in lakes %

1942

0,4

0,8

1,0

1,2

1,4

1,6

L (mm)

% 1962 + glut herring (Alosa aestivalis) 0,2

0,4

0,8

1,0 L

(mm)

From Brooks et Dodson (Science, 1965) 34

Respective effects of competition and predation on size structure of zooplankton communities

•  Brooks & Dodson (1965): « Size-efficiency hypothesis » 1. Competitive superiority of large herbivorous zooplankton 2. Selective predation of large zooplankton by vertebrate predators

35

Size efficiency hypothesis: competitive superiority of large herbivorous zooplankton

Threshold food concentration

The threshold food concentration, necessary to assure that assimilation equals respiration, is lower for the large-bodied species than it is for the small-bodied species under steady-state and low-mortality conditions. Daphnia species

Size at birth (mm)

Size at maturity (mm)

Threshold concentration (µg C L-1)

D. ambigua

0.4

0.8

47

D. galeata

0.6

1.2

43

D. pulicaria

0.7

1.6

30

Daphnidae body size

experimental data from eight filter-feeding species (family Daphnidae) (Gliwicz 1990) and 3 Daphnia species (Kreutzer & Lampert 1999), that strongly support the cornerstone assumption of the competitive aspect of the size-efficiency hypothesis.

36

Gliwicz Z. M.(1990). Food thresholds and body size in cladocerans. Nature 343: 638-640.

Kreutzer C. & W. Lampert (1999). Exploitative competition in differently sized Daphnia species: a mechanisitic explanation. Ecology 80: 2348-2357.

Respective effects of predation by invertebrate and vertebrate organisms on size structure of zooplankton communities

•  Dodson (1974, Ecology): « alternative hypothesis » 1. Selective predation of small zooplankton by invertebrate predators. 2. Selective predation of large zooplankton by vertebrate predators.

37

Selective predation on zooplankton and filtering capacity of herbivorous zooplankton

Highly edible: < 30 µm

(From Burns C. W. (1968) Limnology & Oceanography

Poorly edible: ≥ 30 µm

Mesocosm experiment on Lake Créteil

38

Theoretical prey-dependent models When supposing that it is possible to segregate species within a food web into distinct trophic levels, the response of a given trophic level to an increase of the limiting resource for primary producers, depends upon the number of trophic levels (see Oksanen et al. 1981. Am. Nat. 118)

Trophic level Phytoplankton Zooplankton Planktivorous fish Piscivorous fish

Number of levels 1 2 3 4 















  39

Bottom-up and top-down control of body size within food webs

%

1942

Zooplankton body length

%

1962 (+ glut herring)

Zooplankton body length

From Brooks & Dodson (Science, 1965)

Selectivity of herbivores (From Burns C. W., Limnol. Oceanogr., 1968)

40

Construction of functional food webs of intermediate complexity

Omnivorous invertebrates

Simplified pelagic food web based on functional groups (“trophic species”), differentiated according to body size.

Small herbivorous zooplankton

Small phytoplankton

(Modified from Carpenter et Kitchell, 1993, The trophic cascade in lakes, Cambridge University Press)

Planktivorous fish

Large herbivorous zooplankton

Large phytoplankton

Dissolved nutrients

Inedible algae

41

Mathematical model

Experimental results Taking in account body size allows better accordance between theoretical predictions and observations (From Hulot, Lacroix, Lescher-Moutoué & Loreau, Nature, 2000)

42

Experimental results

Mathematical model

Taking in account body size allows better accordance between theoretical predictions and observations (From Hulot, Lacroix, Lescher-Moutoué & Loreau, Nature, 2000)

43

From individual behaviours to complex community patterns and size-dependent responses of ecosystem functions 44

A useful tool for analysing food-web changes: food-web topology Neo Martinez, www

A simplified food web from the Northern Atlantic (www.ifaw.org)

Can we extract general patterns from topological complexity of natural food webs?

45

Topological analysis

•  Specific richness: S •  Number of feeding links: L •  Link density: L/S •  Connectance: C = L/S2 (ratio of realized feeding links compared to the maximum theoretical number of links ) •  Chain length (mean, min., max.) •  Omnivory and generality indices of species or functional groups •  Mean species trophic position •  Basal, intermediate and top-species…

46

From theory to experimentation Elaboration of theoretical food webs (« Cascade model», « niche model ») and comparison to empirical food webs •  •  •  •  • 

Poor knowledge of real food webs Species aggregation into vague categories (« kind of organisms ») Pooling of data on several dates and sites Comparison of systems with strong dissimilarities in nature, scale, and details Scarce use of experimental approaches for testing theories

47

From theory to experimentation Elaboration of theoretical food webs (« Cascade model», « niche model ») and comparison to empirical food webs •  •  •  •  • 

Poor knowledge of real food webs Species aggregation into vague categories (« kind of organisms ») Pooling of data on several dates and sites Comparison of systems with strong dissimilarities in nature, scale, and details Scarce use of experimental approaches for testing theories

Experimental approaches on aquatic food webs •  •  •  •  • 

Food webs often described at the species level Identical rules across the data set Food webs close to natural ones Large variety of controlled factors Important source of data sets for testing theories on food-web architecture Mesocosm experiment on Lake Créteil (Paris suburb)

48

Effect of foraging behaviour of top species on food-web topology Mesocosm experiment on the effects of biomass and foraging behaviour of two planktivorous fishes Particulate feeder

Lepomis machrochirus (Bluegill, Centrarchidae)

Filter feeder

Dorosoma cepedianum (Gizzard shad, Cupleidae)

49 Lazzaro, Lacroix, Gauzens, Gignoux & Legendre (2009). Journal of Animal Ecology

Contrasted topological characteristics

Topological variable

Visual feeder

Filter feeder

Probability of absence of effect

Richness

-

+

0.0004

Number of basal species

-

+

0.009

Number of herbivorous species

-

+

0.0001

Number and % of top species

-

+

0.0001

Mean /max chain length

+

-

0.0001 / 0.0006

Number of chains

-

+

0.0001

Number of links (link density)

-

+

0.0001

L/S and connectance

-

+

0.0001 / 0.0002

Number of edible algal species

-

+

0.0001

Number and % of algal inedible species

+

-

0.0001

Invertebrate / food-web omnivory index

-

+

0.0005 / 0.0003 50

Lepomis machrochirus (grasper) Dorosoma cepedianum (filter feeder)

51

Functional patterns revealed by the analysis of instantaneous trophic networks, really observed in the experimental enclosures X17taille 25

25

P = 0,007 15

15

Potential network in the enclosures if all species initially present develop and coexist

c

10

10

5

5

0

0

A chlorophyl

Chlorophyll a (µg L-1)

20

20

0

0

20 20

40 40

% of inedible basal species

60 60

Percentage of poorly edible algae

%80

Realized (instantaneous) food web in enclosures after a specific treatment

52

An important limitation: defining food webs Extreme difficulty for constructing matrices: - several dozens to several hundreds of species - Several hundreds of trophic links - Moderate help expected from specific feeding experiments - Moderate benefits expected from tracers

⇒  Creation of a general database on trophic links within freshwater and marine communities -  Freshwater or marine systems -  Qualitative or quantitative data on feeding links -  Prey size (weight), predator size (weight) or prey/predator size ratio. -  Characterization of taxa (taxonomy, life-history and functional traits, etc.) -  Characterisation of ecosystems (country, latitude, longitude, ecosystem type) and environmental conditions (t°C, season, period of the day, light…) -  Introduction of the data sources…

53

A never ending story…

Database Aquaticweb in 2018: - 19605 feeding links arising from 617 scientific articles

Punctual information on: - 2 empires (Prokaryota, Eukaryota) - 3 domains (Bacteria, Archaea, Eukarya) - 6 kingdom - 44 phyla - 100 classes - 275 orders - 713 families - 1229 genera - 1627 species

54

Behaviour of consumers and predator size prey size relationships

Possibility of determining statistically the probability of links from: - The feeding behaviour of consumer -  The size ratio of the studied taxa

55

Towards weighted predator-prey matrices

Establishment of predator-prey weighted matrices from : -  Consumer and prey specificities -  Species biomasses - Consumer size and behaviour and predator /prey size ratio - Life history traits other than body size Improvement compared to the most frequently used theoretical food webs models such as the niche model (Williams & Martinez, Nature, 2000) - More realistic weighted models Study of the role of interaction strength knowing that: - Food webs are dominated by weak links - Interaction strength seems to affect food-web stability

56

A metabolic theory of ecology

•  Basal metabolic rate = fundamental constraint that underpins many size-related patterns and processes in ecology: Towards a metabolic theory of ecology (Brown et al., 2004, Ecology) •  Body size = means of integrating approaches based on biomass and energy flux with those based on abundances and populations. 57

Body size, abundance patterns and structure of food webs

Food web of Broadstone Stream in England

Food web of Tuesday Lake in the USA

Food web of Ythan Estuary in Scotland

Trivariate relationships between log10 body mass, log10 abundance and trophic links. Basal species are shown in green, intermediate species in bleue, and top-species in red. The three Food webs on the same figure suggest the occurrence of strong metabolic constrains. (From Woodward et al. 2005. Body size in ecological networks. Trends in Ecology and Evolution 20: 402-409).

58

From topological networks to energy fluxes Body size involved in many biological processes and energy fluxes at all level of organization. Allometric scaling For a given property Y of an organism of mass M: Y = Y0Mb. log Y = Log Y0 + b log M Slope b constant for a given property

(From Woodward et al. 2005. TREE 20: 402-409)

=> variability of Y0 according to specific features of organisms (e.g. sit-and-wait predators versus active foragers)?

59

Integrating energy fluxes and nutrient constraints

Possibility of lumping species a posteriori into trophic groups (necessity of defining appropriate algorithms for minimizing loss of information)

-  Dynamical models with fluxes of energy and matter transfers -  Stoichiometric characteristics (C:N:P ratios) of trophic species 60

100

****

****

80

****

60 40

****

20

C - Connectance

NC - Number of chains

Food-web architecture and species lumping

species

0.04

species genera functional groups

genera functional groups

***

0.4 ***

****

0.3 0.2 0.1

Gw - Food-web generalism index

0.5

Ow - Food-web omnivory index

**** ***

0.00

0

0.0

descriptors strongly depend upon species lumping.

0.12 0.08

6

4

bluegill (visual feeder)

**** **** ****

2

0 species genera functional groups

-  Absolute values of food-web

species genera functional groups

gizzard shad (filter feeder)

-  Response patterns of food-web descriptors robust to taxonomic and functional aggregation of species. ⇒  New analyses on the interaction effects between visual and filter feeders. ⇒  Large differences in foraging behaviours are mainly expressed at the level of functional groups.

61 Gauzens et al. 2014, Oikos

Elaboration of algorithms for simplifying networks

Mesocosm food web defined at the species levels

62 Mesocosm food web defined at the trophic groups level (groups of species interacting with similar prey and predators)

Mesocosm food web defined as a set of distinct modules (main vertical pathways of energy flow)

Gauzens et al. 2015, Journal of the Royal Society Interface

Supplementary information for people who are interested on the potential importance of neglected interaction links

An example with epibionts of zooplankton

63

From complex to simple networks: what is the importance of neglected interactions? (a)

(b) (c)

3 basic ways for studying a complex network (a): - to aggregate it into a smaller network of larger units (b) - to focus on a sub-graph (c)

(d) - to identify and focus on its most critical nodes (d)

From Jordán (2009). Phil. Trans. R. Soc. B

What is the importance of neglected interactions on our understanding of ecosystem functioning?

64

Epibionts Organisms that live attached to the body surface of other organisms (hosts or basibionts) for a fraction or the totality of their life Various epibionts on zooplankton (bacteria, fungi, ciliates, algae, rotifers, etc.)

Algae BASE

Al-Dhaheri & Willey (1996)

Silnews 61 2012

65

Epibionts of zooplankton Anecdotal information on zooplankton epibionts until the review paper of Threlkeld et al. (TREE, 1993) -  Article oriented towards the interest of epibiont communities as experimental systems for examining the organization of meta-communities

Bottom-up and top-down control Reduced prevalence of epibionts in presence of planktivores suggesting selective removal of zooplankton with epibionts. -  No clear characterization of the effects of predators on epibionts and their hosts. -  No clear information on the role of resources on epibionts -  No clear information on the consequences of epibiosis on ecosystem functioning -  No replicated experimental test

66

Responses of populations of the mixotrophic flagellate Colacium attached on Diaphanosoma Counting of 121,703 cells of Colacium sp. on 631 individuals of Diaphanosoma Brachyurum

Colacium sp. (20 µm) Mixotrophic flagellate (Euglenophyceae) Picture from Al-Dhaheri & Willey (1996). J. Phycol. 32: 770-774

Diaphanosoma brachyurum (Cladocera, 310-1100 µm)

67

Factorial mesocosm experiment 27 10-m3 Enclosures

Nutrients (N1, N2) x Fish (F0, F1, F2, F3) x 3 replicates

Nutrients N0 = N1 = N2 =

0.0 µg P L-1 d-1 0.0 µg N L-1 d-1 L-1

d-1

0.32 µg P 6.4 µg N L-1 d-1 3.20 µg P L-1 d-1 64.00 µg N L-1 d-1

Fish F0 = 0 fish enclosure-1 F1 = 1 roach (0+) enclosure-1 F2 = 2 roach (0+) enclosure-1 F3 = 4 roach (0+) enclosure-1

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Epibiont burden depends upon zooplankton groups

-  Colacium epibionts are more abundant on large zooplanktonic crustacea (in particular Cladocera such as Diaphanosoma) -  Some preference patterns appear to be independent upon body size: •  Burden much more lower on Calanoida than on similar-sized Cyclopoida) •  Burden higher on Diaphanosoma than on similar-sized Daphnia

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Mean of Ln Colacium / individual ± SEM

Responses of populations of the mixotrophic flagellate Colacium attached on Diaphanosoma N0 N1 N2

N: P = 0.9 F: P = 0.0001 (N x F): P = 0.10 Similar negative effect of fish on large zooplankton: - Cladocera - invertebrate carnivores (data not shown)

F0

F1

F2

F3

Epibiosis: Protection against invertebrate predators Supply of hot spots of resources for mixotrophic epibionts Increased exposure to fish predation (because of greater visibility or reduction of host swimming ability) is a potential cost for both host and epibionts

“shared doom’’ effect” sensu Wahl (J. Anim. Ecol. 2008)

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Responses of populations of the mixotrophic flagellate Colacium attached on Diaphanosoma

Ln (epibionts + 1)

Abundance of Colacium sp. According to fish treatment and body size of Diaphanosoma

F0 F1 F2 F3

Standardized values ​of logarithms of body length of Diaphanosoma (310 - 1100 µm)

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Effects of epibiosis on the community structure of pelagic primary producers Possibility of estimating the importance of epibionts within communities of pelagic primary producers by using specific epibiont burdens and abundances of zooplankton groups

72 communities of pelagic primary producers dominated by: -  planktonic cells in systems dominated by planktivorous fish -  attached cells in systems without fish or dominated by piscivorovous fish?

Conclusion Colacium appear to be totally independent upon dissolved nutrients: - Hosts suppliers of resources (hot spots) for these mixotrophic organisms Very high abundances of attached epibionts attached on large zooplankton in fishless systems - Protection against predation by invertebrates Very strong negative effect of fish on both large zooplankton and epibionts: - Shared-doomed effect

Major changes in community structure of pelagic primary producers associated to almost neglected interaction networks between epibionts and their hosts Interest of coupling various types of interaction networks 73

Conclusions And perspectives

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Towards more realistic food webs Static topological food-web models may be revisited by: -  Working on realised instantaneous networks -  Switching from binary topological food webs to weighted networks, -  Better generalizing interactions between predator behaviour and prey:predator size ratios -  Integrating density-dependence in link probability -  Taking into account species plasticity -  Integrating allometric rules -  Lumping species for developing more adapted dynamical models

Aquatic systems are particularly well suited for such studies

Biodiversity and ecosystem functioning: Perspectives and challenges Scaling-up in space and time Most experiments were made on small spatial and temporal scales. Need of larger-scaled experiments. 1. Role of biodiversity as an assurance against unpredictable catastrophic events? 2. Biodiversity and community invasion resistance? 3. Effect of diversity loss at local and regional space? (need of a theory on meta-ecosystem functioning) 75

Biodiversity and ecosystem functioning: Perspectives and challenges Linking biodiversity dynamics and ecosystem functioning 1. How global changes affect biodiversity, ecosystem functioning, and the interaction between them? 2. Separate and interaction effects of biotic and abiotic factors? 3. Evolutionary constraints, trade-off, biodiversity, and ecosystem functioning? 4. Natural selection of ecosystem properties? 76

Experimental facilities of PLANAQUA (Anaee-France / H2020 AQUACOSM network)