Food Web Structure in Antarctica in a Context of Global Climate Change: a Stable Isotope Perspective

Home , Adamussium, Odontaster validus, Sterechinus neumayeri

Food web structure in Antarctica in a context of global climate change: a stable isotope perspective

Loïc N. MICHEL, Bruno DANIS, Philippe DUBOIS, Marc ELEAUME, Jérôme FOURNIER, Cyril GALLUT, Philip JANE & Gilles LEPOINT Contact: [email protected]

Course "Etude des isotopes stables et applications au milieu marin" Sea ice in Antarctica

Sea ice is a major environmental driver of ecological processes in Antarctica . Water column mixing . Benthic-pelagic coupling . Niche partitioning . Benthic community structure . …

Image: NASA Sea ice in Antarctica

Sea ice is a major environmental driver of ecological processes in Antarctica . Water column mixing . Benthic-pelagic coupling . Niche partitioning . Benthic community structure . …

Sea ice is a highly dynamic system

Image: NASA Seasonal patterns of sea ice cover

Source: NOAA

Austral winter Austral summer Normal cycle: Thick sea ice cover Thinning and breakup of sea ice Changes in Antarctic sea ice cover

Climate change causes contrasted changes in sea ice cover in Antarctica

Spatial extent Changes in sea ice concentration

From King (2014), Nature 505: 491-492. (Data 1979-2012) Changes in Antarctic sea ice cover

Climate change causes contrasted changes in sea ice cover in Antarctica

Spatial extent Temporal extent Changes in sea ice concentration Changes in sea ice season duration

West Antarctic Peninsula

From King (2014), Nature 505: 491-492. From Massom & Stammerjohn (2010), Pol . Sci. 4: 149-186 (Data 1979-2012) (Data 1979 -2004) Study site: Dumont d’Urville station Austral summer 2007-08

East Antarctica, Adélie Land Petrels Island Study site: Dumont d’Urville station Austral summer 2007-08

Austral summer 2013-14 East Antarctica, Adélie Land Petrels Island

2013-2015: Event of high spatial and temporal sea ice coverage

No seasonal breakup during austral summers 2013-14 and 2014-15 Study site: Dumont d’Urville station Time of sampling : Austral summer 2014-15

This is the sea (Please trust me) Study site: Dumont d’Urville station Time of sampling : Austral summer 2014-15

This is the sea (Please trust me)

How will benthic communities respond to sudden changes in sea ice cover? How could increased sea ice cover impact structure of benthic food webs? Food web structure in natural ecosystems

Food web: natural interconnection of food chains and a graphical representation of what- eats-what in an ecological community. Network formed by entirety of trophic interactions found in a given ecosystem.

Food webs are complex ecological networks, but a lot of that complexity can be summarized using two dimensions, leading to their classical depiction as 2D diagrams

Charles Sutherland Elton (1900-1991) Summerhayes & Elton (1923): J. Animal Ecol. 11(2): 216-233 Food web structure in natural ecosystems

Phytoplankton Benthic biofilm + Sea ice algae detritus Food web structure in marine ecosystems

Horizontal dimension

Phytoplankton Benthic biofilm + Sea ice algae detritus Resources supporting the consumers Food web structure in marine ecosystems

Horizontal dimension

Vertical dimension Trophic position of the consumers the of position Trophic

Phytoplankton Benthic biofilm + Sea ice algae detritus Resources supporting the consumers Food web structure in marine ecosystems

Horizontal dimension

Vertical dimension

Here: models based on trophic markers (stable isotope ratios) were used to as proxies of both food webs dimensions

Horizontal dimension: use of a mixing model (SIAR) to identify main food items of consumers

Trophic position of the consumers the of position Trophic Vertical dimension: use of a trophic position model (tRophicPosition)

Phytoplankton Benthic biofilm + Sea ice algae detritus Resources supporting the consumers Sampling: under ice SCUBA diving Sampling: food items

1. Sympagic algae

2. Suspended particulate organic matter (SPOM) Sampling: food items

3. Benthic brown algae Himantothallus grandifolius Sampling: food items

4. Benthic biofilm (heterogeneous mix of microalgae, bacteria, amorphous material and detrital items) Some sampled consumers Perkinsiana sp. Flabelligera mundata

Harmothoe sp.

O. validus is usually bright to dull red on the dorsal (abactinal) surface and yellowish white to pale pink on the ventral (actinal) surface [16]. O. meridionalis is generally pale brown or yellowish white on the dorsal : surface and lighter on the ventral surface [16]. Color in both spAmmotheaecies can be highly variacarolinensisble and is not always reliable as a field character; the only sure way is to check the number of spines on the actinal plates [16].

Here's a juvenile and adult of Odontaster validus. Size-frequency distribution of O. Heterocucumis sp. Sterechinus neumayeri validus can vary with location and is a reflection of the general level of productivity of a habitat: at McMurdo Station, their size and number decrease with depth; at Cape Evans, they are more numerous and generally smaller; and, at East Cape Armitage, they are less numerous and very small [3]. O. validus is slow growing; well-fed individuals need about nine years to reach thirty grams wet weight which is near the mean size of shallow-water individuals at McMurdo Station [3]. Based on its growth rate, collected sizes, and knowledge from other seastars, O. validus may live beyond one hundred years of age, with very low turnover in a population [17].

Odontaster validus Hemigellius sp.

27 Some sampled consumers Perkinsiana sp. Flabelligera mundata

Harmothoe sp.

Adamussium colbecki seastar Odontaster validus Odontaster validus is found throughout Antarctica and the Marseniopsis sp. Antarctic Peninsula, South Shetland Islands, South Orkney Islands, South Sandwich Islands , South Georgia Island,Trophon Shag longstaffi Rocks, Marion and Prince Edward Islands, and Bouvet Island at depths from 0 to 914 meters [7,10,11,12,14]. O. validus is the most abundant seastar in the shallow shelf waters of Antarctica and is most abundant from 15 to 200 meters [9]. O. validus has a broad disc and short arms tapering to blunt tips [7]. O. validus has been collected at sizes up to seven centimeters in radius from its center to the tip of an arm [7,11]. O. validus varies in color including dark brown, purple, purple-red, orange, red-orange, red, brick red, dark carmine, and pink; it may have light colored arm tips [7,11,14]. O. validus has a characteristic position with its arm tips slightly raised In total: 28 taxa (9 phyla, all present functional[7]. guilds) O. validus is usually bright to dull red on the dorsal (abactinal) surface and yellowish white to pale pink on the ventral (actinal) surface [16]. O. meridionalis is generally pale brown or yellowish white on the dorsal : surface and lighter on the ventral surface [16]. Color in both spAmmotheaecies can be highly variacarolinensisble and is not always reliable as a field character; the only sure way is to check the number of spines on the actinal plates [16].

Odontaster validus Hemigellius sp.

27 Material & methods: analysis University of Liège’s setup: Vario MICRO cube EA coupled to an Isoprime 100 IRMS Results: isotopic biplot

1 0 F o o d ite m s S P O M B io film H im a n to th a llu s b la d es S y m p a g ic a lg a e

)

‰

(

N 6

1 

2 -2 5 -2 0 -1 5 -1 0 1 3  C (‰ ) Results: isotopic biplot

1 0 Perkinsiana sp. F o o d ite m s S P O M B io film H im a n to th a llu s b la d es S y m p a g ic a lg a e

8 P o lych a e te s H a rm o th o e sp . F la b e llig e ra m u n d a ta Harmothoe sp. P o lyc irru s sp .

P e rk in sia n a sp .

)

‰

(

N 6

1 

Flabelligera mundata

2 -2 5 -2 0 -1 5 -1 0 1 3  C (‰ ) Results: isotopic biplot

1 0 Trophon longstaffi F o o d ite m s S P O M B io film H im a n to th a llu s b la d es S y m p a g ic a lg a e

8 P o lych a e te s H a rm o th o e sp . F la b e llig e ra m u n d a ta P o lyc irru s sp . P e rk in sia n a sp .

) M o llu scs

‰ ( T ro p h o n lo n g s ta ffi

N 6 5

1 M a rsen io p sis sp .  L a te rn u la e llip tic a A d a m u ssiu m c o lb e c k i

Marseniopsis sp.

2 Adamussium colbecki -2 5 -2 0 -1 5 -1 0 1 3  C (‰ ) Results: isotopic biplot

1 0 HeterocucumisF o o d ite msps . S P O M B io film H im a n to th a llu s b la d es S y m p a g ic a lg a e

P o lych a e te s 8 seastar Odontaster validus H a rm o th o e sp .

Odontaster validus is found throughout Antarctica and the F la b e llig e ra m u n d a ta Antarctic Peninsula, South Shetland Islands, South Orkney Sterechinus neumayeri Islands, South Sandwich Islands , South Georgia Island, Shag Rocks, Marion and Prince Edward Islands, and Bouvet Island at P o lyc irru s sp . depths from 0 to 914 meters [7,10,11,12,14]. O. validus is the most abundant seastar in the shallow shelf waters of Antarctica and is P e rk in sia n a sp . most abundant from 15 to 200 meters [9]. O. validus has a broad disc and short arms tapering to blunt tips [7]. O. validus has been

) collected at sizes up to seven centimeters in radius from its center to the tip of an arm [7,11]. O. validus varies in color includingM darko llu scs

‰ brown, purple, purple-red, orange, red-orange, red, brick red, dark

( [7,11,14] carmine, and pink; it may have light colored arm tips . O. T ro p h o n lo n g s ta ffi validus has a characteristic position with its arm tips slightly raised

N 6 [7]

5 .

1 M a rsen io p sis sp .

 O. validus is usually bright to dull red on the dorsal (abactinal) surface and yellowish white to pale pink on the ventral (actinal) L a te rn u la e llip tic a surface [16]. O. meridionalis is generally pale brown or yellowish white on the dorsal : surface and lighter on the ventral surface [16]. Color in both species can be highly variable and is not always reliable as a field character; the only sure way is to check the number of spines on the actinal plates [16]. A d a m u ssiu m c o lb e c k i

Here's a juvenile and adult of OdontasterE c h in o d e rm s validus. Size-frequency distribution of O. validus can vary with location and is a reflection of the general level of O p h iu ra sp . productivity of a habitat: at McMurdo Station, their size and number decrease S te re c h in u s n e u m a ye ri 4 with depth; at Cape Evans, they are more numerous and generally smaller; and, at East Cape Armitage, they are less D ip la steria s b ru c ei numerous and very small [3]. O. validus is slow growing; well-fed individuals need O d o n ta ste r v a lid u s about nine years to reach thirty grams wet weight which is near the mean size of shallow-water individuals at McMurdo H e te ro c u c u m is sp . Station [3]. Based on its growth rate, collected sizes, and knowledge from other S ta u ro c u c u m is sp . seastars, O. validus may live beyond one hundred years of age, with very low turnover in a population [17].

Odontaster validus

-2 5 -2 0 -1 5 -1 0 27 1 3  C (‰ ) Results: isotopic biplot

1 0 F o o d ite m s S P O M B io film H im a n to th a llu s b la d es S y m p a g ic a lg a e

8 P o lych a e te s H a rm o th o e sp . F la b e llig e ra m u n d a ta P o lyc irru s sp . P e rk in sia n a sp .

) M o llu scs

‰ ( T ro p h o n lo n g s ta ffi

N 6 5

1 M a rsen io p sis sp .  L a te rn u la e llip tic a A d a m u ssiu m c o lb e c k i

E ch in o d e rm s O p h iu ra sp .

4 S te re c h in u s n e u m a ye ri D ip la steria s b ru c ei O d o n ta ste r v a lid u s H e te ro c u c u m is sp . S ta u ro c u c u m is sp .

2 -2 5 -2 0 -1 5 -1 0 1 3  C (‰ ) Results - SIAR modelling Sympagic

algae diet Suspended Particulate Organic Matter (SPOM)

Contribution to consumer to consumer Contribution Benthic algae + Biofilm

OV: O. validus; SN: S. neumayeri; DB: D. brucei; HA: Harmothoe sp.; FM: F. mundata; PO: Polycirrus sp.; OP: Ophiura sp.; PE: Perkinsiana sp.; TL: T. longstaffi; MA: Marsienopsis sp.; HE: Heterocucumis sp.; LE: Laternula elliptica; AC: Adamussium colbecki; ST: Staurocucumis sp. Results - SIAR modelling Sympagic

algae diet Suspended Particulate Organic Matter (SPOM)

Contribution to consumer to consumer Contribution Benthic algae + Biofilm

algae diet Suspended Particulate Organic Matter (SPOM)

Contribution to consumer to consumer Contribution Benthic algae + Biofilm

algae diet Suspended Particulate Organic Matter (SPOM)

Contribution to consumer to consumer Contribution Benthic algae + Biofilm

1000 km

Main food items SympagicSympagicalgaealgae BenthicBenthicalgaealgae// Biofilm Biofilm

DDU Discrepancies in resource use Species DDU 1 2 3 4 5 6 Laternula elliptica Adamussium colbecki Sterechinus neumayeri Odontaster validus Staurocucumis sp. Harmothoe sp.

1000 km 6 Main food items 5 Sympagic algae / Ice POM Benthic algae / Biofilm Plankton / SPOM Sediment POM

Animal-based diet 4 1-3 No data References: 1-3: Norkko et al. 2007 Ecology 88: 2810-2820; 4: Gillies et al. 2012 Estuar Coast Shelf S 97: 44-57; 5: Dunton 2001 Amer Zool 41: 99-112; 6: Corbisier et al. 2004 Polar Biol 27: 75-82 DDU Discrepancies in resource use Species DDU 1 2 3 4 5 6 Laternula elliptica Adamussium colbecki Sterechinus neumayeri Odontaster validus Staurocucumis sp.

Harmothoe sp.    1000 km Sea ice 6 Main food items 5 Sympagic algae / Ice POM Benthic algae / Biofilm Plankton / SPOM Sediment POM

Harmothoe sp.    1000 km Sea ice 6 Main food items 5 Sympagic algae / Ice POM Benthic algae / Biofilm ImportantPlankton / spatial SPOM and/or temporal variation in resource use by dominant consumers Sediment POM Animal-basedHighdiet trophic plasticity of Antarctic invertebrates? 4 1-3 No data References: 1-3: Norkko et al. 2007 Ecology 88: 2810-2820; 4: Gillies et al. 2012 Estuar Coast Shelf S 97: 44-57; 5: Dunton 2001 Amer Zool 41: 99-112; 6: Corbisier et al. 2004 Polar Biol 27: 75-82 DDU Sympagic algae consumption: how and why? Sea ice is a dynamic system: constant melting/freezing

Sympagic algae aggregates sink quickly

Sinking speed is size-dependent and range from 100 to 500 m/day (i.e. 1-5 hours to reach a depth of 20 m) Sympagic algae consumption: how and why? Sea ice is a dynamic system: constant melting/freezing

Sympagic algae aggregates sink quickly

Sinking speed is size-dependent and range from 100 to 500 m/day (i.e. 1-5 hours to reach a depth of 20 m)

Why is it preferred by many consumers over more 8 abundant food items such as biofilm?

a r

Better nutritional value? Unlikely… 

N / C 6 Better palatability? Pure aggregates of microalgae… 5

4 S y m p . a lg a e B io film Role of benthic biofilm in the food web Preliminary microscopic examination: Benthic biofilm = heterogeneous mix of microalgae, amorphous material and detrital items

Here: importance of benthic biofilm in food web comparatively limited despite high abundance Role of benthic biofilm in the food web Preliminary microscopic examination: Benthic biofilm = heterogeneous mix of microalgae, amorphous material and detrital items

Here: importance of benthic biofilm in food web comparatively limited despite high abundance

Ross Sea: Benthic invertebrates consume more detritic matter in sea-ice influenced locations (Norkko et al. 07) Role of benthic biofilm in the food web Preliminary microscopic examination: Benthic biofilm = heterogeneous mix of microalgae, amorphous material and detrital items

Here: importance of benthic biofilm in food web comparatively limited despite high abundance

Ross Sea: Benthic invertebrates consume more detritic matter in sea-ice influenced locations (Norkko et al. 07)

Important variation in benthic ecosystem response to sea ice: sudden changes vs. stable conditions? However: no data about dynamics of biofilm accumulation! Here: long-lived benthic invertebrates with low metabolic rates  low isotopic turnover? Is isotopic equilibrium reached? Our model could underestimate actual biofilm importance for invertebrate feeding Results: full community

1 2

S a lia ste ria s b ra c h ia ta A c o d o n ta ste r s p . Iso te a lia a n ta rc tic a D e c o lo p o d a a u stra lis 1 0 A m m o th e a c a ro lin e n s is P a rb o rla s ia c o rru g a tu s

)

‰

(

1 

2 -2 5 -2 0 -1 5 -1 0 1 3  C (‰ ) Image: NASA Vertical dimension – Trophic position modelling Overall: low trophic positions compared

to literature

Trophic position Trophic

brucei

australis

longstaffi

brachiata

antarctica

neumayeri

Ophiura

carolinensis

Acodontaster

Trophon

Diplasterias

Odontaster validus Odontaster

Isotealia

Decolopoda

Saliasterias

Sterechinus

Parborlasia corrugatus Parborlasia Ammothea Vertical dimension – Trophic position modelling Overall: low trophic positions compared to literature

Dominant omnivore taxa: very low trophic levels, mostly feeding directly

on primary Trophic position Trophic

producers

brucei

australis

longstaffi

brachiata

antarctica

neumayeri

Ophiura

carolinensis

Acodontaster

Trophon

Diplasterias

Odontaster validus Odontaster

Isotealia

Decolopoda

Saliasterias

Sterechinus

Parborlasia corrugatus Parborlasia Ammothea

The food web we expected Trophic position of the consumers the of position Trophic