The Ecology of Whale Falls at the Deep-Sea Floor

Craig R. Smith, Amy R. Baco, Adrian Glover, and many others

Acknowledgments: NURC-Alaska, NSF, National Geographic Society, BBC

Michael Rothman

Outline:

a. Whales as extreme detritus

b. Approach for studying whale falls

c. Community succession

d. Endemic species and whaling

e. Biotechnological spinoffs

f. Conclusions

Typical Deep-Sea Floorenergy-poor “desert”

Sulfide-rich hydrothermal vent, Galapagos Spreading Center with giant bivalves (Calyptogena pacifica) & tubeworms (Riftia pachyptila)

21 m blue whale skeleton, 1240 m Santa Catalina Basin

~ 1 m

1987 Santa Catalina Basin

1240 m

Known distribution of Whale-fall Communities (n ~ 30 for modern whale falls, and n = 24 for fossil whale falls up to 30 million yr old)

5

8

2

>20

Fossil whale comms.

3

12

Characteristics of dead whales (largest detrital particles):

1) Massive, 40 ton whale contains

- 2 x 106 g Corg

2) High in quality (largely blubber, protein, oily bones)

3) Typically sink to a very food-poor deep-sea floor

Sediments underlying abyssal whale fall (50 m2) –

sustain 4000-yr of background labile Corg flux

Goals of our whale-fall studies:

1) Evaluate deep-sea community response to an intense pulse of organic enrichment

2) Elucidate the importance of whale falls as organic- and sulfide-rich habitat islands

ALVIN

Advanced Tethered Vehicle

Tiburon

0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19

Years Since Located at Seafloor

San Diego Trough

San Clemente Basin

San Nicolas

Santa Cruz Basin

Santa Catalina Basin

1987

1988

1991

1995

1999

2004

1995

1995

2000

1996

1997

1998

1998

1999

1999

2002

2004

2005

2004

2005

We predicted that deep-sea whale falls pass through three successional stages:

1) A Mobile Scavenger Stage

2) An Enrichment Opportunist Stage

3) A Sulfophilic (“Sulfide-Loving”) Stage

Species structure, duration, vent-seep affinities?????

First will

SHOW VIDEOS

to illustrate successional stages

General pattern has emerged concerning:

- community structure

- duration

- vent-seep affinities

MOBILE SCAVENGER STAGE

n = 2

- 5000 kg gray whale in San Diego Trough

- 25,000 kg gray whale in Santa Cruz Basin

Michael Rothman

25 ton gray whale at 1.5 mo – 1674 m Santa Cruz Basin

Summary of Mobile scavengers on 25,000 kg Santa Cruz Carcass at

t = 1.5 monthsSpecies Abundance Biomass (kg)

Eptatretus deani(hagfish)

400 – 800 40 – 80

Lysianassid amphipod (crustaceans)

105 – 106 ? 10 –100 ?

Somniosus pacificus (sleeper

shark)1 - 3 50 - 1000

Totals 105 – 106 ? 100 - 1200

Mobile Scavenger Stage Duration?

25 ton carcass

1.5 mo – Largely Intact

18 mo – Skeletonized!

- 5 ton carcass stripped in ~ 4 mo

Duration ~ 4 – 18 mo(30-60 kg tissue removed per day)

- High abundance of generalized scavengers (hagfish, sleeper sharks, stone crabs, amphipods)

- Scavenging rates of 30-60 kg per day

- 38 species attracted, but no whale-fall specialists

- No apparent overlap with permanent vent-seep faunas

CHARACTERISTICS OF MOBILE-SCAVENGER STAGE

ENRICHMENT OPPORTUNIST STAGE

n = 3

- 5000 kg gray whale in San Diego Trough

- 10,000 kg gray whale San Clemente Basin

- 25,000 kg gray whale in Santa Cruz Basin

Michael Rothman

Santa Cruz carcass – 18 mo

Sediment Macrofauna at Santa Cruz Whale Fall – 18 mo

NU

MB

ER P

ER M

2

SULFIDE AND Corg IN TOP 2 CM

0

2

4

6

8

10

12

0 5 10 15 20 25 30 35

DISTANCE FROM WHALE (m)

Sulfide

% Organic Carbon

SULF

IDE

(mM

) or C

org

(%)

DOMINANT INFAUNAL SPECIES

0

5000

10000

15000

20000

25000

0 5 10 15 20 25 30 35

DISTANCE FROM WHALE (m)

Hyalogyrina sp. n.

Bivalve juv sp. A

Cumella sp. A

Ophryotrocha sp. n.

Ampharetid sp. A

Cumacean sp. K

Cirratulid sp. A

Evolutionary noveltiesCarpet worm = Vigtorniella flokati

- new to science

- reduced gut

- bizarre behavior

- only found at whale falls

Santa Cruz Basin – 1670 m

Bone-eating siboglinid snot worms > 16 species

Monterey Canyon - O. rubiplumus & O. frankpressi(Rouse et al. 2004)

Sweden – Osedax mucofloris(Glover et al., 2005)

Santa Cruz Basin -Osedax new species

World Wide Whale Worms?

Japan -Osedax new species

- no gut or mouth

- bacterial “root garden” for eating whale oil

- a new feeding mode and type of bacterial symbiosis

Evolutionary novelty:

(Goffredi et al., 2005, Goffredi and Smith, unpublished)

Summary of Enrichment Opportunist Stage for 5000 – 25,000 kg carcasses

-Rapid colonization by enrichment generalists (Cumella) and whale fall specialists(?) (Vigtorniella, Osedax)

-Pattern reminiscent of enrichment communities in shallow water (e.g., near sewer outfalls)

-Duration of stage: < 3.2 yr for 5,000 kg carcass, > 4.5 yr for 25,000 kg carcass

-Potential for some affinities to vent-seep fauna (bivalve juveniles, dorvilleids)

SULFOPHILIC STAGE (“sulfur loving”)

n = 4

- 10,000 kg gray whale San Clemente Basin

- 25,000 kg gray whale Santa Cruz Basin

- ~40,000 kg baleanopterid San Nicolas slope

- 70,000 kg baleanopterid Santa Catalina Basin

Michael Rothman

Santa Cruz Basin – 4.5 yr

Santa Catalina Basin carcass at

39 yr

Mats of sulfur oxidizing bacteria

Clams with chemo-autotrophic endosymbionts

1 cm

Idas washingtonia and Cocculina craigsmithi

60% lipid (fat)

0.1 % lipid (fat)

Taxon San Clemente(3.4 yr)

San Nicolas (70 yr)

Santa Catalina (54 yr)

MytilidIdas washingtonia > 20,000 > 10,000 > 10,000

LimpetsCocculina craigsmithi - 300 1,100Pyropelta corymba - 1,200 1,000Pyropelta musaica - 280 1,000Other Limpets - 1,800 1,200

SnailsMitrella permodesta 3? 1,800 1,800Provanna lomana - 1,500 -Eulimella lomana ~1,000 - -Juveniles and Others 1,800 1,700 800

CrustaceansIllyrachna profunda 900 500 1,800Amphipods < 400 800 500Galathaeids 800 ~50 ~100Misc. Crustaceans 9,000 8,000 4,000

PolychaetesNereid sp. 1 ~50 ~50 ~50Ampharetids 50? 2,500 100Misc. polychaetes 1,800 10,000 8,000

Total Individuals >40, 000 >40,000 > 30,000Total Species >103 >201 >180

Estimated Population Sizes of Whale-Fall Fauna in Sulfophilic Stage

Among most biodiverse deep-sea hard substrates (> vents)

HYPOTHESIS:

Whale falls serve as dispersal stepping stones for species dependent on sulfur-based chemoautotrophy at the deep-floor.

Smith et al., 1989

Species Whale Sk. Guay. Vents JdF Vents NEP Seeps GOM SeepsBIVALVES Vesicomya gigas ++ ++ ++

Calyptogena kilmeri + ++Calyptogena elongata + + ++Calyptogena pacifica? ++ ++ ++Idas washingtonia ++ + + +

GASTRO. Pyropelta corymba ++ +Pyropelta musaica ++ + ++Cocculina craigsmithi ++ + +Neoleptopsis sp.? + +Astyris permodesta ++ +Provanna lomana ++ ++Eulimella lomana ++ + ++

ISOPODS Illyrachna profunda ++ +Janiridae sp. + ++

AMPHIPODS Seba profunda ++ +POLYCH. Bathykurila guaymasensis + +

Syllid sp. A + ++Sabellid sp. A + +Maldanid sp. C + +Dorvelleid sp. + +Scale Worm sp. ++ +

VESTIMENT. Escarpia spicata + + ++ +ENTOPROCTS Entoproct sp. B + +TOTALS VENTS 11 SEEPS 19

Species Overlap With Other Sulfide-Rich Habitats

Species Population Size Collection SitesPOLYCHAETES Vigtorniella flokati 1000 - 100,000 California, Hawaii

Palpiphitime n. sp. >10,000 California, SwedenHarmothoe craigsmithi ? CaliforniaPenialopolynoe santacatalina ? CaliforniaAmpharetid n. genus >10 CaliforniaAsabellides n. sp. >10 CaliforniaAnobothrus n. sp.Osedax 7 spp. Spionid

?>1000-10,00

>10000

CaliforniaCalifornia, Sweden, Japan

Mont Canyon

~ 8 Dorvilleid species 100s – 1000’s California

CRUSTACEANS Paralomis manningi ? CaliforniaSeba n. sp. 100s California

APLACOPHORAN New genus ? CaliforniaBIVALVES Adipicola pelagica ? South Atlantic

Adipicola osseocola ? New ZealandMyrina pacifica ? Japan, Hawaii

Idas arctuatilis ? New ZealandIdas pelagica ? North AtlanticIdas ghisotti ? North Atlantic

GASTROPODS Bruciella laevigata ? New ZealandBruciella pruinosa ? New ZealandXylodiscula osteopelta ? New ZealandPyropelta wakefieldi 100’s California

SIPUNCULAN Phascolosoma saprophagicum 10’s – 100’s New Zealand

TOTAL > 36

SPECIES KNOWN ONLY FROM WHALE FALLSARE THERE WHALE-FALL SPECIALISTS?

Consequences of whaling?

- Vast reduction in abundance of live whales & whale-fall habitats at the deep-sea floor.

- North Atlantic – 75% reduction? (Roman & Palumbi, 2003)

- Global Sperm whales ~ 65% reduction(Whitehead, 2002)

North Atlantic great whales?(Romand & Palumbi, 2003)

Sustainable yield level (IWC)

N.B. Metapopulation models yield similar predictions

Whale specialist extinction as a function of habitat loss, based on species-areas relationships (e.g., Nifle and Mangel, 2000)

Conclusions:

1) Whales falls play a surprising role in deep seafloor ecosystems providing –

- organic and sulfide-rich habitat islands (and stepping stones?),

- hotspots of biodiversity and evolutionary novelty,

- unique niches for a potentially large number of whale-fall specialists.

2) By drastically reducing the number of whale falls, whaling may cause significant species extinctions at the deep-sea floor.