FLOATING SEAWEED AS EPHEMERAL

NEUSTONIC HABITATDrijvend zeewier als efemeer neustonisch habitat

Sofie Vandendriessche

The neustonic zone and its inhabitants

Neuston s.l.: all plants and animals inhabiting the surface layer of oceans and seas

Pleuston = organisms whose bodies project at least partly into the air (Physaliaphysalis = Portuguese-Man-of-War; the water bug Halobates sp.) Neuston s.s. = organisms that live underneath the water surface film (e.g.Janthina sp. = purple bubble raft snail)

Sampling: neuston net that partly projectsabove and below the water surface=> Neuston s.l.

www.jochemnet.de

FLOATING SEAWEED AS EPHEMERAL NEUSTONIC HABITAT

? ? ?

The neustonic zone and its inhabitants

Harsh environment:high temperature variation high UV irradiation high light levels inhibit photosynthesis exposed to wave actionmarine and aerial predators contaminants (heavy metals, hydrocarbons)

The neustonic layer: considerably different living conditions compared to deeperlayers

Rich environment:High dissolved oxygen contentIntensive absorption of solar radiationHigh nutrient supply

airial precipitationanimal excreta and remainscolloidal and dissolved organic matter

Floating tar

Foam

Whale carcass

Rich fauna displaying adaptive strategies to reduce stress (e.g. pigmentation, floating devices)

Floating objects

Why do neustonic organisms concentrate near floating objects?

Availibility of a surface for attachmentProvision of shelter from predatorsPresence of a food source

Substitution of the seabedSpawning substrate and nursery areaMeeting point for the formation and maintenance of schoolsCleaning station

Possibility for dispersal via rafting

Small-scale spatial variation in neuston: local accumulations of organisms

< winds and currents, which create surface slicks, fronts, upwelling zones and windrows

< presence of floating structures (seaweed, wood, plastic debris, buoys, pumice,...)

Floating objects

Song Ye et al, 1991 – Minchin, 1996 - Jokiel, 1989 – Thiel, 2003 - Barnes & Fraser, 2003

Low food valueHigh survival time

High food valueLow survival time

High food valueHigh survival time

Natural Man-made

Tar pellets, plastic, rubber, rope, nylon nets, bottles

Less photodegradableResurfaceNo grazing

Tar from natural seepsVolcanic pumice

SeedsLogsseagrass

seaweed

GrazingDegradationpneumatocysts

Grazing Degradation

FLOATING SEAWEED AS EPHEMERAL NEUSTONIC HABITAT

?

Pelagic Sargassum versus ephemeral seaweed aggregations

Sargassum natans & S. fluitans in the Atlanticocean

Fully adapted to a permanently pelagic life

Rich fauna :

- Specialised / endemic e.g. Histrio- Opportunists: juvenile fish, invertebrates, young turtles looking for food and shelter

Multi-species

aggregates of detached intertidal and subtidal seaweed branches

< fragmentation due to storms, grazing damage & seasonal release of plant parts

limited longevity => ephemeral

Associated fauna

www.bigelow.org

Ephemeral rafts of floating seaweed

Fauna on seaweed rafts (Thiel & Gutow, 2005)

Species composition of seaweed-associated fauna

4 categories influences

1) Inhabitants of attached seaweeds2) Inhabitants of cast-up seaweed3) Subtidal, benthic and epibenthic species4) Planktonic and neustonic species

Clump sizeSpatial and temporal variationRaft age (succession)Seaweed species compositionDisturbance and exchange between clumps

Objectives and thesis outline

Ecological impact of floating seaweeds as ephemeral habitats in the North Sea?

Influence of floating seaweed on the richness and composition of the neuston

Analysis of the environmental and biological factors structuring the seaweed-associated invertebrate community

Effect of increased prey concentration on the presence, abundance and behaviour of fishes and birds

Seaweed raft longevity and potential as dispersal vector

I.

Chapter 2. Floating seaweed in the neustonic environment: a case study from Belgian coastal waters

II.

Chapters 3 - 4. Food and habitat choice in floating seaweed clumps: the obligate opportunistic nature of the associated macrofauna & Sources of variation in floating seaweed associated macro-invertebrates

III.

Chapters 5 -6. Hiding and feeding in floating seaweed: floating seaweed as possible refuges or feeding grounds for fishes & Seabirds foraging at floating seaweeds in the Northeast Atlantic

IV.Chapter 7. Floating seaweed and the influences of temperature, grazing and clump size on raft longevity – a microcosm study

Hiding and feeding in floating seaweed: floating seaweed clumps as possible refuges and feeding

grounds for fishes

Floating seaweed clumps as refuges or feeding grounds for fishes

Wide variety of fish taxa are attracted to floating structures

Plastic debris, floating seaweeds, wood, jellyfish, FAD’s, animal remainse.g. Safran & Omori, 1990; Davenport & Rees, 1993; Moser et al, 1998, Masuda & Tsukamoto, 2000; Castro et al, 2002; Jacquemet, 2004; Thiel & Gutow, 2005a; Thiel & Gutow, 2005b

Fish community most diverse underneath seaweeds (Fedoryako, 1989):increased diversity due to the substantial increase in habitat complexity of the pelagic environment due to the presence of these seaweeds Kingsford (1995)

AIMS:describe species composition and behaviour of fish associated with

floating seaweedscomparing neustonic data with those obtained from seaweed samplessize distributions and diets of the fishesstructuring factors influencing species composition

Provision of food, shelter, a visual orientation point, passive transport, ...

Gathering data: sampling along the Belgian coast

Dip net samples

Seaweed-associated fish

Neuston net samples

Neustonic fish

length rangeSP SU AU WI (cm)

Ammodytes tobianus /Hyperoplus lanceolatus

Arnoglossus laterna ∎ 0,5 1Belone Belone ∎ 0,9 - 3,7 69

Chelon labrosus ∎ ∎ ∎ 0,3 - 3,8 1591Ciliata mustela ∎ ∎ 0,4 - 3,6 405

Clupea harengus /Sprattus sprattus/

Engraulis encrassicolusCottidae sp. ∎ ∎ ∎ 0,2 - 1,2 290

Echiichthys vipera ∎ 0,4 - 1,6 45Hippocampus guttulatus ∎ 2,9 - 3,5 2

Labrus bergylta ∎ 0,6 - 1,1 2Merlangius merlangus ∎ 0,6 - 4,1 10

Pleuronectidae sp. ∎ ∎ 0,7 - 1,3 3Pollachius pollachius ∎ 3,2 1

Pollachius virens ∎ 2,5 1Scophthalmus maximus ∎ ∎ 1,6 - 2,1 4

Solea solea ∎ ∎ ∎ ∎ 0,3 - 0,8 14Syngnathus acus ∎ ∎ ∎ 2,9 - 5,5 7

Syngnathus rostellatus ∎ ∎ ∎ ∎ 1,0 - 5,7 28Trachurus trachurus ∎ ∎ 0,3 - 4,2 258

0,4 - 9,3 2257∎ ∎ ∎ ∎

# caught

∎ ∎ ∎ ∎ 0,3 - 12,2 884

Significant seasonal differences

MDS of neustonic fish data (sqrt transformation, Bray-Curtis similarity): black triangles = summer samples, white triangles =autumn samples, crosses = spring samples, squares = winter samples

Stress: 0,13

large variability in the summer samples (average similarity: 34), compared to the other seasons (average similarity au: 64, wi: 54, sp: 60).

No effects of sampling station and presence of small amounts of floating seaweed and debris

Neustonic fish

Length range # caughtSP SU AU WI (cm)

Belone belone ∎ 4.0 1Blennidae ∎ 1 – 1.2 2

Callionymus lyra ∎ - 1Chelon labrosus ∎ ∎ 0.7-2.8 202Ciliata mustela ∎ ∎ 1.0 - 4.0 147

Cottidae ∎ 0.8 – 1.7 13Cyclopterus lumpus ∎ ∎ ∎ ∎ 0.6 – 4.9 97Entelurus aequorius ∎ ∎ ∎ 13.6 - 15 6

Gobiidae ∎ 1.1 – 1.2 2Merlangius merlangus ∎ 3.4 1

Nerophis lumbriciformis ∎ 5 1Pollachius pollachius ∎ 2.3 – 2.6 11

Pollachius virens ∎ 2.3 1Syngnathus acus ∎ 7.4 - 14.4 2

Syngnathus rostellatus ∎ 3.7 – 12.2 7Trachurus trachurus ∎ 0.7 – 4.3 147

Stress: 0,01

Chelon labrosus

Cyclopterus lumpus

Ciliata mustela Trachurus trachurus

Groups based on dominant fish species

pattern of the fish data compared to the environmental data: seaweed volume, relative abundances of the seaweed constituents per sample, surface water temperature and salinity, distance to shore, atmospheric pressure and humidity, densities of seaweed-associated macrofauna

Low matching coefficient (0.23): only part of biotic structure explained

Seaweed-associated fish

Seaweed-associated fish

Harpacticoida L. holsatus MG G. crinicornis /G. locustaI. baltica H. varians PL Idotea sp. JP. longicornis MG C. maenas MG L. holsatus JAphididae S. marina A. swammerdamiP. elegans PL Jassa sp. ChironomidaeI. emarginata T. tergipes

Cyclopterus lumpus

0204060

0,5-1 1-1,5 1,5-2 2-2,5 2,5-3 3-3,5 3,5-4 4-4,5 4,5-5

length class (cm)

# in

divi

dual

s

Ciliata mustela

-150-100-50

050

100

0 - 0,5 0,5 - 1 1 - 1,5 1,5 - 2 2 - 2,5 2,5 - 3 3 - 3,5 3,5 - 4

length class (cm)

# in

divi

dual

s

Chelon labrosus

-150

-100

-50

0

50

100

0 - 0,5 0,5-1 1-1,5 1,5-2 2-2,5 2,5-3 3-3,5 3,5-4

length class (cm)

# in

divi

dual

s

Trachurus trachurus

-150

-100

-50

0

50

0 - 0,5 0,5 - 1 1 - 1,5 1,5 - 2 2 - 2,5 2,5 - 3 3 - 3,5 3,5 - 4 4 - 4,5

length class (cm)

# in

divi

dual

s

Syngnathus rostellatus

-15

-10

-5

0

5

1 - 1,5 2,5 - 3 4-4,5 5,5-6 7-7,5 8,5-9 10-10,5 11,5-12

length class (cm)

# in

divi

dual

s

Black: seaweed fishGrey: neustonic fish

Seaweed-associated fish: size-frequency distributions

Numerical percentage

0%

20%

40%

60%

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100%

1,5 - 2 2 - 2,5 2,5 - 3 3 - 3,5 3,5 - 4

le ngt h c la ss (cm)

L. ho lsatus MG unid ent . Crab larvae Gammarus sp .

Calano id a sp . Harp actico id a sp . I. b alt ica

fish egg A. swammerdami G. crinico rnis / G. locus tares t

• First-year juveniles

• Highest Fulness index (0 – 18.3), positively correlated with length of the fish• Shift in dominant prey with increasing length: Liocarcinus holsatus megalopae, calanoid and harpacticoid copepods and small gammarid amphipods (mainly Gammarus sp. juveniles) in the smallest length class Idotea baltica, fish eggs, calanoids and large gammarid amphipods (Gammarus locusta and G. crinicornis) in the larger length classes

Stomach analyses of 5 fish species: Cyclopterus lumpus

Stomach analyses of 5 fish species

TRACHURUS TRACHURUSNume ric a l pe rce nt a ge

0%

20%

40%

60%

80%

100%

2 - 2,5 2,5 - 3 3 - 3,5 3,5- 4

lengt h c la sse s

L. holsa t us Z Ca la noida sp. Ha rpa c t ic oida sp.

P a la e monida e sp. Z Cypris Biva lvia

P odon sp. Mysida ce a sp. Na uplius

Nume ric a l pe rc e nt age

0%

20%

40%

60%

80%

100%

2 - 2,5 2,5 - 3 3 - 3,5

le ngt h c la sse s

Ca la noida sp. Ha rpa c t ic oida sp. P a la emonidae sp. P L

P a la e monida e sp. Z Cypris P le urobrac hia pile us

Ga mma rus sp.

Neuston Seaweed

SYNGNATHUS ROSTELLATUS< 8 cm : only calanoid copepods

> 8 cm from seaweed samples also ingested harpacticoid copepods and crab megalopae

Seaweed fish: calanoid (N%: 95) and harpacticoid copepods (N%: 3.9), dipteraninsects (N%: 0.6).Neustonic fish: Calanoid copepods (N% >99); Dipteran insects and cypris larvae were rarely found; harpacticoid copepods were absent

CILIATA MUSTELA Nume ric a l pe rce nt a ge

0%

20%

40%

60%

80%

100%

2 - 2,5 2,5 - 3 3 - 3,5

le ngt h c la sse s

L. holsa t us MG Ca la noida sp. f ish e gg

P la t he lmint he s Ammodyt ida e sp.

Nume ric a l pe rce nt a ge

0%

20%

40%

60%

80%

100%

2,5 - 3 3 - 3,5 3,5 - 4

le ngt h c la sse s

L.holsa t us MG Cala noida sp. inve rt ebra t e egg

f ish e gg Harpac t icoida sp. Ga mma rus sp.

re st

Neustonic fish: Calanoida, fish eggs and, as they grow, they start feeding on larger prey items like crab megalopae. Seaweed-associated fish: more variable, also comprises harpacticoid copepods, small gammaridamphipods and invertebrate eggs (probably from isopods and amphipods).

CHELON LABROSUS

Stomach analyses of 5 fish species

Neustonic fish community Seaweed-associated fish community

Mainly seasonally structured Low matching coefficient with environmental data, seaweed composition, associated macrofaunal densities

Fish do not select their seaweed clumps

Individuals captured from below floating seaweeds are often larger than conspecifics from open waters (Kingsford, 1992)

Chelon labrosus Cyclopterus lumpus, Trachurus trachurus, Ciliata mustela: effect of species interactions (competition, territorialism)?

Obvious in all species, especially Ciliata mustela and Syngnathus rostellatus

protection and/or food enhance growth OR floating seaweeds are colonised by larger individuals

Conclusions

Cylopterus lumpus:

only found in seaweed samples, majority of ingested prey consists of seaweed-associated fauna (gammarid amphipods, idoteid isopods, crab megalopae, postlarval prawns, harpacticoids)

weedpatch specialist: closely associated resident

Ciliata mustela & Trachurus trachurus

larger individuals in seaweed clumps, ingestion of seaweed associated macrofauna (limited proportion of diet)

visitors – residents

Chelon labrosuscomparable size as in neuston, very limited feeding on associated fauna

(only harapacticoids)visitors

Syngnathus rostellatus

recruitment from neuston or carried with seaweed

Conclusions

“Floating seaweeds can be regarded as temporary and unpredictablehabitats shared between several fish species (mainly juveniles) that use

them for different reasons and with variable intensity.”

Seabirds foraging at floating seaweeds in the Northeast Atlantic

photo: I. Hinojosa & M. Thiel

Introduction

Variations in seabird distribution:

Large scale Environmental heterogeneity due to physical oceanographic processes

Pervasive anthropogenic disturbance

Patchiness Species-specific responses to the environmente.g. surface features can provide resting grounds or additional food

Fronts, internal wavesFloating objects such as plastic, cuttlebones, seaweed

Are there seabirds that are frequently observed in association with ephemeral seaweed patches?

Are these associations feeding mode dependent?

database analysis

ESAS – European Seabirds at Sea

Seabird observations collected and coded using standardised survey techniques

Used data from North Sea, period 1979 -2000Specific coding for associations birds and surface phenomena

Floating seaweeds as sources of small-scale patchiness in seabirds

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Parasitism, scavenging, opportunistic surface feeding

Surface-seizing, pursuit-plunging, pursuit-diving (shallow dives)

Surface feeding, dive down to 5-10 m

Deep diving, pelagic and bottom feeding

Diving, benthos feeding

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surface peckingActively searchingPursuit plunging

Arctic TernSurface pecking, actively searching and dipping => dipping and surface pecking

Sandwich Tern:Actively searching & deep plunging

Common Tern:Actively searching, pursuit diving & scavenging =>surface pecking and

dipping

Floating seaweeds as sources of small-scale patchiness in seabirds

Other clues about the association seabirds – floating seaweeds from literature:

Terns: plunge-diving in vicinity of floating seaweeds in Canada (Parsons, 1986)

Roosting and foraging in South Africa and Sargasso Sea (Tree & Klages, 2004, Haney, 1986)

Fulmars: Idotea metallica in diet (Furness & Todd, 1984)

Pecking on North Sea debris (Cadée, 2002)

Cormorants: Pick up floating debris from sea-surface (Tasker et al, 2000)

Cyclopterus lumpus in diet (Lilliendahl & Solmundsson, 2006)

Common scooters and eiders: mainly benthos feeders, but also feed on seaweed-associated organisms

Some seabirds are attracted to floating seaweeds

Mostly plunge-diving or surface feeding

Profit from increased prey concentration

The increased structural complexity and food supply in floating seaweeds temporarily enhance foraging conditions for some seabirds depending on their preferred prey and foraging strategy small-scale patchiness

photo: I. Hinojosa & M. Thiel

An interest for floating objects may be lethal

Photo: F. & K. Starr