Download Three-year investigations into sperm whale

Marine Ecology. ISSN 0173-9565
ORIGINAL ARTICLE
Three-year investigations into sperm whale-fall ecosystems
in Japan
Yoshihiro Fujiwara1, Masaru Kawato1, Tomoko Yamamoto2, Toshiro Yamanaka3, Waka Sato-Okoshi4,
Chikayo Noda1,5, Shinji Tsuchida1, Tomoyuki Komai6, Sherine Sonia Cubelio1,7, Takenori Sasaki8, Karen
Jacobsen9, Kaoru Kubokawa10, Katsunori Fujikura1, Tadashi Maruyama1, Yasuo Furushima1, Kenji
Okoshi11, Hiroshi Miyake1,12, Masayuki Miyazaki1, Yuichi Nogi1, Akiko Yatabe1,7 & Takashi Okutani1
1 Extremobiosphere Research Center, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), 2-15 Natsushima-cho, Yokosuka,
Kanagawa, Japan
2 Faculty of Fisheries, Kagoshima University, 4-50-20 Shimoarata, Kagoshima, Japan
3 Department of Evolution of Earth Environments, Graduate School of Social and Cultural Studies, Kyushu University, Ropponmatsu, Chuo-ku,
Fukuoka, Japan
4 Graduate School of Agricultural Science, Tohoku University, 1-1 Amamiya-machi, Tsutsumidori, Aoba-ku, Sendai, Miyagi, Japan
5 Graduate School of Biosphere Science, Hiroshima University, 1-4-4 Kagamiyama, Higashi-Hiroshima, Japan
6 Natural History Museum and Institute, Chiba, 955-2 Aoba-cho, Chuo-ku, Chiba, Japan
7 Tokyo University of Marine Science and Technology, 4-5-7 Konan, Minato-ku, Tokyo, Japan
8 The University Museum, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo, Japan
9 In Situ Scientific Illustration, Ketchum, ID, USA
10 Center for Advanced Marine Research, Ocean Research Institute, The University of Tokyo, 1-15-1 Minamidai, Nakano-ku, Tokyo, Japan
11 Faculty of Science and Technology, Ishinomaki Senshu University, 1 Shinmito, Minamisakai, Ishinomaki, Miyagi, Japan
12 Enoshima Aquarium, Katasekaigan, Fujisawa, Kanagawa, Japan
Keywords
Adipicola pacifica; chemosynthetic
community; succession; sulfide concentration;
Whale fall.
Correspondence
Yoshihiro Fujiwara, Extremobiosphere
Research Center, Japan Agency for MarineEarth Science and Technology (JAMSTEC),
2-15 Natsushima-cho, Yokosuka, Kanagawa
237-0061, Japan.
E-mail: [email protected]
Accepted: 21 December 2006
doi:10.1111/j.1439-0485.2007.00150.x
Abstract
We report the first study of sperm whale-fall ecosystems, based on mass sinking of whale carcasses at shelf depths in the northwest Pacific. We conducted
three observations over a 2-year period on replicate sperm-whale carcasses
implanted at depths of 219–254 m off the southern part of Japan from July
2003 to August 2005. The study was made possible by a mass stranding of
sperm whales in January 2002, and the subsequent sinking of 12 carcasses in
the waters off Cape Nomamisaki. Dense aggregations of unique chemosynthesis-based fauna had formed around the whale carcasses after 18 months (July
2003). The mytilid mussel Adipicola pacifica was the most abundant macrofaunal species and covered most of the exposed bone surfaces. The general composition of the fauna was similar to that of deep-water reducing habitats, but
none of the species appearing in this study has been found at hydrothermal
vents, cold seeps or deep-water whale falls. A new species of lancelet, which
was the first record of the subphylum Cephalochordata from reducing environments, a new species of Osedax; a rarely encountered benthic ctenophore, and
a rare gastropod species were discovered at this sperm whale-fall site. Benthic
communities were similar across all the carcasses studied, although the body
sizes of the whales were very different. The succession of epifaunal communities was relatively rapid and the sulphophilic stage was considerably shorter
than that of other known whale falls.
Marine Ecology 28 (2007) 219–232 ª 2007 The Authors. Journal compilation ª 2007 Blackwell Publishing Ltd
219
Sperm whale-fall ecosystems in Japan Fujiwara, Kawato, Yamamoto, Yamanaka, Sato-Okoshi, Noda, Tsuchida, Komai, Cubelio, Sasaki, Jacobsen, Kubokawa, Fujikura, Maruyama, Furushima, Okoshi, Miyake, Miyazaki, Nogi, Yatabe & Okutani
Problem
The first discovery of a whale-fall in situ occurred in 1987
in the Santa Catalina Basin, California at a depth of
1240 m (Smith et al. 1989). A large chemosynthetic
assemblage was reported around the whale carcasses
(Smith et al. 1989), with similarities to hydrothermal vent
and cold-seep communities. Since this discovery, many
whale-fall communities have been reported, including
modern and fossil assemblages (Smith & Baco 2003).
Whale falls have been thought to be ‘stepping stones’ not
only for dispersal of deep-sea chemosymbiotic species but
also for the introduction over evolutionary time of chemoautotrophy-dependent invertebrates to vent and seep
environments (Smith et al. 1989; Distel et al. 2000).
A mass stranding of 14 sperm whales (Physeter macrocephalus Linnaeus, 1758) occurred on the southwestern
coast of Kyushu Island, southern Japan, on January 22,
2002. The bodies of 12 whales were sunk by local government authorities in the waters off Cape Nomamisaki,
southwestern tip of Kyushu Island, at depths of 200–
300 m on February 1, 2002.
Most ecological studies of whale falls have been conducted on baleen whale carcasses off California, at depths
of 1000–2000 m (Smith & Baco 2003). No sperm whale
falls and related biological assemblages have been discovered before this mass sinking, although this whale species
should be sufficiently large to sustain whale-fall-specific
biological assemblages. In addition, sperm whales have an
oil-rich structure known as the spermaceti organ that
takes up 25–33% of the animal’s body (Whitehead 2003).
This unusual organ might serve as a unique habitat for
whale-fall specialists.
The sperm whale falls off Cape Nomamisaki were
located in waters shallower than most previously studied
whale falls. The only whale-fall community reported shallower was at 125 m in the North Sea (Glover et al. 2005).
The whale bone-eating siboglinid worm Osedax mucofloris
was the most abundant species on the North Sea skeleton
(Glover et al. 2005). It was not clear whether mass aggre-
gation of chemosymbiont-bearing invertebrates occurs at
shallow-water whale falls, as on deep-water falls.
While many whale-fall communities have been reported
from the northeast Pacific, limited whale-fall information
is available from the northwest Pacific. The only whalefall community reported from this region was on the Torishima Seamount at a depth of 4037 m (Fujioka et al.
1993; Wada 1993). The skeleton had already been eroded
heavily by the time of discovery. Unidentified mytilids,
tubicolous polychaetes and galatheid crabs were abundant
(Naganuma et al. 1996).
There have been no previous observations of multiple
large whale carcasses implanted simultaneously in a specific limited area. The largest whale sunk off Cape Nomamisaki was twice as heavy as the smallest. The
influence of whale body size on the formation and succession of biological assemblages could thus be investigated.
The aims of this study were to (1) clarify whether
sperm whale carcasses, like those of baleen whales, sustain
chemosynthetic communities, (2) characterize the macrofaunal assemblages on whale falls in relatively shallower
water in the northwest Pacific, (3) investigate the ecological differences between whale-fall communities on carcasses of varying size, and (4) document patterns of
ecological succession in shallow-water whale-fall communities.
Material and Methods
Site survey and sampling
The carcasses of 12 sperm whales were loaded on barges
and sunk by local government authorities in the waters
off Cape Nomamisaki, southwestern tip of Kyushu Island,
at depths of 200–300 m on February 1, 2002 (Table 1,
Fig. 1). The whales had decomposed internally but the
external morphology was not severely damaged. Each
whale was wrapped in nylon net (mesh size: approximately 10 cm). As ballast, six to thirteen concrete blocks
(approximately 2.5 tons each) were attached to each
Table 1. Whale falls investigated in this study. These specimens were dropped off Cape Nomamisaki, Japan, on February 1, 2002.
whale total length estimated weight depth latitude
no.
(m)
(t)
(m)
(N)
2
6
7
11
12
13.20
16.00
12.95
13.05
13.50
23.0
39.0
21.9
22.3
24.5
219
228
229
245
254
31
31
31
31
31
23.865¢
20.998¢
20.720¢
18.844¢
18.515¢
longitude
(E)
129
129
129
129
129
58.766¢
59.158¢
59.285¢
59.520¢
59.374¢
dive no./year
July 2003
July 2004
July–August 2005
198
—
462
191, 196
329, 331, 332
452, 456
189, 190, 192, 193, 197 328, 329, 331, 332 453, 457, 464, 465
—
333
458
194, 195
330
459, 463, 466
Whale numbers indicate the order of dropping to the seafloor. Whale lengths were provided by the local government and their weights were estimated according to Lockyer (1976). Geographic positions were calculated according to the World Geodetic System 1984 (WGS84). Dive numbers
of the ROV Hyper-Dolphin are shown at each whale-fall site.
220
Marine Ecology 28 (2007) 219–232 ª 2007 The Authors. Journal compilation ª 2007 Blackwell Publishing Ltd
Fujiwara, Kawato, Yamamoto, Yamanaka, Sato-Okoshi, Noda, Tsuchida, Komai, Cubelio, Sasaki, Jacobsen, Kubokawa, Fujikura, Maruyama, Furushima, Okoshi, Miyake, Miyazaki, Nogi, Yatabe & Okutani
Sperm whale-fall ecosystems in Japan
JAPAN
km
0
50
Kyushu Isl.
Tubeworm Site
Cape Nomamisaki
Kagoshima Bay
2
6&7
11&12
Fig. 1. Location of whale falls (solid circles:
no. 2, 6, 7, 11 and 12) studied off Cape
Nomamisaki, Japan. The locations of Cape
Nomamisaki and Kagoshima Bay are
indicated. The ordinate is in degrees north
latitude and the abscissa in degrees east
longitude. Open circle indicates the habitat of
Lamellibrachia satsuma at the depth of 80 m.
2006 Sep 06 17:47:43
whale using wire rope. Five of the whales were subsequently studied using the remotely operated vehicle
(ROV) Hyper-Dolphin in 2003, 2004 and 2005 (Table 1).
Ten dives were conducted in July 2003 (dives no. 189–
198), six dives in July 2004 (dives no. 328–333) and eleven dives in July–August 2005 (dives no. 452, 453, 456–
459, 462–466). Biological and geochemical samples were
collected using manipulators, a scoop-sampler, a suction
sampler and sediment corers installed on the ROV. Whale
bones were collected using manipulators and stored in a
sample box or a sample basket. Most epifaunal species
were collected using a suction sampler, and sedimentdwelling infauna were collected using a scoop-sampler.
Biological sorting was conducted using three sieves with
different mesh sizes (0.5, 1 and 2 mm). Taxonomic identifications were made using collected specimens (except
for some large species mentioned in Tables 2–5) by
T. Okutani and T. Sasaki for mollusks; W. Sato-Okoshi &
K. Fujikura for polychaetes; S. Tsuchida, T. Komai and
S. S. Cubelio for crustaceans; H. Miyake for ctenophores;
K. Kubokawa for cephalochordates; and T. Okutani and
Y. Fujiwara for the remainder. Sediment samples were
collected using PVC tube corers (7 cm in diameter,
28 cm in length). Core samples of bones were collected
from vertebrae using an electric hole saw (3 cm in diameter, 30 cm in length). Water temperature was measured
using the SBE 19 CTD profiler (Sea-Bird Electronics,
Washington, USA).
Quantitative sampling and measurements of shell length of
Adipicola species
Quadrat sampling (quadrat size: 25 and 100 cm2) of
Adipicola pacifica was conducted quantitatively on the
surfaces of recovered whale bones. Three sets of quadrat
samples were obtained in July 2003, five sets in July 2004
and four sets in July 2005. The total number and wet
weight (including shells) of A. pacifica collected from each
Marine Ecology 28 (2007) 219–232 ª 2007 The Authors. Journal compilation ª 2007 Blackwell Publishing Ltd
221
Sperm whale-fall ecosystems in Japan Fujiwara, Kawato, Yamamoto, Yamanaka, Sato-Okoshi, Noda, Tsuchida, Komai, Cubelio, Sasaki, Jacobsen, Kubokawa, Fujikura, Maruyama, Furushima, Okoshi, Miyake, Miyazaki, Nogi, Yatabe & Okutani
Table 2. Molluscan fauna associated with all the sperm whale falls
investigated.
Bivalvia
Gastropoda
Scaphopoda
Cephalopoda
no. of taxa
Solemya pervernicosa
Adipicola crypta
Adipicola pacifica
Atrina teramachii
Chlamys empressae
Chlamys lemniscata
Lucinoma adamsianum
Wallucina sp.
Nitidotellina soyoae
Dillwynella vitrea
Homalopoma sp.
Cocculina sp.
Tanea magnifluctuata
Pisanianura breviaxe
Ceratostoma inornata
Mitrella bicincta
Zeuxis castus
Olivella spretoides
Pleurobranchella nicobarica
Striodentalium rhabdotum
Gadilina sp.
Octopus sp.*
22
Table 3. Polychaetous fauna associated with all the sperm whale falls
investigated.
2003
2004
2005
subclass
order
family (species)
2003
2004
2005
+
+
+
+
+
+
+
+
+
+
Scolecida
+
+
+
+
+
+
+
+
Palpata
Capitellidae
Maldanidae
Paraonidae
Orbiniidae
Opheliidae
Polynoidae
Aphroditidae
Nereididae
Glyceridae
Goniadidae
Nephtyidae
Phyllodocidae
Dorvilleidae
Lumbrineridae
Onuphidae
Serpulidae
Siboglinidae
(Osedax japonicus)
Cirratulidae
Acrocirridae
Terebellidae
Spionidae
Apistobranchidae ?
Protodrilidae
23
+
+
+
+
Unplaced
Unplaced
Unplaced
Unplaced
Unplaced
Phyllodocida
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
Eunicida
Sabellida
+
+
+
+
+
8
14
Terebellida
+
14
Spionida
Unplaced
Plus signs indicate the appearance (observed and/or collected) of each
taxon in each year. Specimens collected/observed from all whale carcasses investigated are shown. The total number of taxa appearing in
each year is given on the bottom row. All taxa shown in this table
were collected unless otherwise stated.
*Identified from high-definition TV video.
quadrat was measured. Shell lengths of all A. pacifica
specimens collected for quantitative analyses and all Adipicola crypta collected during all three cruises were also
measured.
Measurement of sulfide concentration in sediments
To measure sulfide concentrations in sediments, acid-volatile sulfide (AVS) was liberated by anaerobic acidification
of cored sediments in 1 n HCl during active distillation
(with pure nitrogen gas) of a ca. 5-cm3 core fraction and
collection of liberated H2S in traps containing cadmium
acetate solution (2.5%), following which the sulfide was
precipitated as CdS. The yellow CdS precipitate was oxidized with a few drops of hydrogen peroxide solution
(34.5%). These resulting sulfates were recovered as BaSO4
after adding BaCl2 solution. The resulting BaSO4 precipitates were precisely weighed and calculated as millimoles
per kilogram of dry sediment (mmÆS2)Ækg)1). Analytical
error associated with the overall process of the AVS determinations was less than 5%.
222
no. of taxa
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
15
+
18
16
+
+
+
+
+
+
+
+
+
+
+
+
+
Plus signs indicate the appearance of each taxon in each year. The
total number of taxa appearing in each year is given on the bottom
row. All taxa shown in this table were collected.
Specimen maintenance in aquaria
One vertebra, one ulna and one epiphysis collected in
July 2004 and three vertebrae collected in July–August
2005 were maintained at JAMSTEC in five air-bubbled
aquaria (approximately 100 l each) containing artificial
Rohtomarine (Rei-Sea, Tokyo, Japan) seawater at 12 C.
The aquarium water was filtered using EHEIM classic or
professional filters (EHEIM GmbH & Co. KG, Deizisau,
Germany) and the seawater was exchanged when the
transparency became low. The salinity was manually controlled at approximately 35& by adding freshwater. No
organic dietary supplements were supplied.
Results
Decomposition of whale carcasses
In July 2003 (1.5 years after emplacement), we visited
four whale carcasses off Cape Nomamisaki, Japan, at
depths of 219–254 m (Table 1, Fig. 1). The seafloor sediment was sandy and the water temperature was 12 C.
The whale carcasses had been largely skeletonized by this
Marine Ecology 28 (2007) 219–232 ª 2007 The Authors. Journal compilation ª 2007 Blackwell Publishing Ltd
Fujiwara, Kawato, Yamamoto, Yamanaka, Sato-Okoshi, Noda, Tsuchida, Komai, Cubelio, Sasaki, Jacobsen, Kubokawa, Fujikura, Maruyama, Furushima, Okoshi, Miyake, Miyazaki, Nogi, Yatabe & Okutani
Sperm whale-fall ecosystems in Japan
Table 4. Crustacean fauna associated with all the sperm whale falls investigated.
subclass/infraclass
Ostracoda
Thecostraca
/Cirripedia
Malacostraca
order/infraorder
Pedunculata
Leptostraca
Amphipoda
Cumacea
Euphausiacea
Decapoda
/Caridea
/Thalassinidea
/Anomura
family
Heteralepadidae
Nebaliidae
Gammaridae
Alpheidae
Hippolytidae
Processidae
Pandalidae
Callianassidae
Diogenidae
Paguridae
Chyrostylidae
Galatheidae
/Brachyura
Homolidae
Dorippidae
Leucosiidae
Majidae
Atelecyclidae
Cancridae
Goneplacidae
Xanthidae
Pinnotheridae
no. of taxa
species
2003
unidentified sp.
+
Heteralepas sp.
unidentified sp.
unidentified sp.
unidentified sp.
unidentified sp.
+
+
+
Alpheus sp. (macrochirus group?)
Eualus sp. cf. kikuchii
Processa philippinensis
Plesionika crosnieri
Plesionika grandis
Callianassa s.l. sp.
Cestopagurus sp. nov.
Paguristes albimaculatus
Nematopagurus lepidochirus
Nematopagurus spinulosensoris
Eumunida sp.
Galathea sp. 1
Galathea sp. 2
Galathea sp. 3
Galathea sp. 4
Munida sp. 1
Munida sp. 2
Munida sp. 3
unidentified sp.
Homola orientalis
unidentified sp.
Ethusa sp.
Cryptocnemus obolus
unidentified sp. 1
unidentified sp. 2
Merocryptus lambriformis
Macrocheira kaempferi*
Pugettia minor
Oxypleurodon stimpsoni
Trachycarcinus sagamiensis
Cancer gibbosulus
Cancer japonicus
Carcinoplax surugensis
Medaeus serratus
unidentified sp.
Pinnixa sp.
42
2004
2005
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
10
+
+
12
+
+
+
+
31
Plus signs indicate the appearance (observed and/or collected) of each taxon in each year. The total number of taxa appearing in each year is
given on the bottom row. All taxa shown in this table were collected unless otherwise stated.
*Identified from high-definition TV video.
time (Fig. 2a and d). Most soft tissues, such as the viscera
and muscle had been consumed, but large amounts of
head and blubber tissue remained. Only the vertebrae of
the largest whale (number 6, total length ¼ 16 m) were
still connected with the soft tissue.
The second whale-fall cruise was conducted 2.5 years
after carcass emplacements (July 2004) (Table 1). The
lower halves of the vertebrae of all skeletons were mostly
buried in the sediment and their spinous processes had
nearly disappeared (Fig. 2b). The skulls had broken down
Marine Ecology 28 (2007) 219–232 ª 2007 The Authors. Journal compilation ª 2007 Blackwell Publishing Ltd
223
Sperm whale-fall ecosystems in Japan Fujiwara, Kawato, Yamamoto, Yamanaka, Sato-Okoshi, Noda, Tsuchida, Komai, Cubelio, Sasaki, Jacobsen, Kubokawa, Fujikura, Maruyama, Furushima, Okoshi, Miyake, Miyazaki, Nogi, Yatabe & Okutani
Table 5. Other remarkable taxa associated with all the sperm whale
falls investigated.
taxa
species
2003 2004 2005
Porifera
Cnidaria
Hydrozoa
Anthozoa
unidentified sp.
unidentified sp.
unidentified sp.
Actiniaria: Unidentified sp.
+
Edwardsia sp.
unidentified sp.
Ctenophora
Lyrocteis imperatoris
Nemertea
unidentified sp.
+
Sipuncula
unidentified sp.
+
Echiura
unidentified sp.
Entoprocta
unidentified sp.
Brachiopoda
unidentified sp.
+
Crinoidea
unidentified sp.
Asteroidea
unidentified sp.
Ophiuroidea
unidentified sp.
+
Phrynophiurida: Unidentified sp.
Echinoidea
unidentified sp.
Holothuroidea
unidentified sp.
+
Cephalochordata Asymmetron inferum
+
Vertebrata
Congridae gen. sp.*
Moridae gen. sp.*
+
Ophidiidae gen. sp.*
Helicolenus hilgendorfi*
+
Sebastiscus tertius*
+
Niphon spinosus*
no. of taxa
25
10
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
15
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
22
Plus signs indicate the appearance (observed and/or collected) of each
taxon in each year. The total number of taxa appearing in each year
is given on the bottom row. All taxa shown in this table were collected unless otherwise stated.
*Identified from high-definition TV video.
considerably (Fig. 2b). The connective tissue between the
vertebrae had disappeared, but large amounts of soft tissue from the skulls and blubber were still present. The
third cruise was conducted 3.5 years after the carcass
sinking (July–August 2005) (Table 1). The bones were
buried deeper in the sediments (Fig. 2c) but the cephalic
soft tissues and some blubber were still present.
Whale bones were sampled during all three cruises.
The vertebrae were relatively solid after 1.5 years but fragile and porous after 3.5 years, with little difference
between individual whale skeletons. Core samples collected from vertebrae after 3.5 years were less oily and malodorous than those collected during the first and second
sampling times.
Biological assemblages around whale carcasses
Dense biological assemblages occurred around sperm
whale carcasses after 1.5 years. A mytilid mussel was the
224
most abundant (Fig. 3) and covered most exposed surfaces of the skulls, ribs, epiphyses and vertebrae. Two
other symbiont-harboring bivalves and a new species of
lancelet were located in sediments underneath the skeletons. A new species of the polychaete in the genus Osedax
inhabited the bones and soft tissues. After 2.5 and
3.5 years, whale carcasses showed higher species richness
(44, 56, and 85 taxa at 1.5, 2.5 and 3.5 years respectively)
and the biomass was the greatest at 1.5-year-old carcasses.
Control sampling of background fauna was conducted
more than 10 m from the carcasses. No species were
shared between the whale falls and background environment.
Molluscan fauna
The molluscan fauna observed/collected at the whale fall
sites is shown in Table 2. The most abundant mollusk
was the mytilid mussel Adipicola pacifica (Dall, Bartsch
& Rehder, 1938), which covered bone surfaces exposed
to seawater. Adipicola pacifica extended its inhalent and
exhalent siphons into the water column (Fig. 3), as
reported by Okutani et al. (2003). Another whale-fall
mussel, Adipicola crypta (Dall, Bartsch & Rehder, 1938)
(Fig. 4a), was also found on the same whale carcasses
but it was attached only to bone surfaces buried in sediments (Fig. 5). The solemyid clam Solemya pervernicosa Kuroda, 1948 was also collected from sediments
beneath the carcasses (Fig. 4b). These three species were
the most abundant bivalves observed throughout the
3.5-year study period. The most abundant gastropod
species at all three sampling times was Dillwynella vitrea
Hasegawa, 1997. Many carnivorous gastropods, such as
Ceratostoma inornata (Récluz, 1851), Tanea magnifluctuata (Kuroda 1961) (Fig. 4c) and Mitrella bicincta (Gould, 1860), were present on 2.5- and 3.5-year-old
carcasses but were rare on 1.5-year-old carcasses.
Ceratostoma inornata was observed to feed on a live
A. crypta in our aquaria.
Polychaetous fauna
Polychaete species collected/observed at the whale-fall
sites are shown in Table 3. The total number of polychaete families was similar among years, but the family identities varied markedly between the 1.5-year and later
sampling times. The Nereididae, Capitellidae and Dorvilleidae constituted more than 70% of total collected polychaete abundance at 1.5-year carcasses. On the other
hand, a protodrilid polychaete was obviously more abundant on the 2.5- and 3.5-year-old ones (Fig. 4d), but population sizes could not be accurately estimated because
the worm was located in small pores of whale bones and
Marine Ecology 28 (2007) 219–232 ª 2007 The Authors. Journal compilation ª 2007 Blackwell Publishing Ltd
Fujiwara, Kawato, Yamamoto, Yamanaka, Sato-Okoshi, Noda, Tsuchida, Komai, Cubelio, Sasaki, Jacobsen, Kubokawa, Fujikura, Maruyama, Furushima, Okoshi, Miyake, Miyazaki, Nogi, Yatabe & Okutani
Sperm whale-fall ecosystems in Japan
(a)
(b)
(c)
Fig. 2. A whale-fall community (whale
number 12, 13.5 m length) at a depth of
254 m off Cape Nomamisaki, Japan. A dense
aggregation of fauna had formed around the
whale skeleton by July 2003. However, by
July 2005 this community was already
beginning to disappear. These images were
taken by the ROV Hyper-Dolphin in (a) July
2003, (b) July 2004 and (c) July 2005.
(d) Schematic drawing of whale no. 12 in July
2003.
(d)
Fig. 3. Living specimens of the mytilid mussel
Adipicola pacifica on a whale vertebra. Both
inhalent and exhalent siphons were extended
into the water, unlike the other mytilids.
was not quantitatively sampled. The collected Cirratulidae, Lumbrineridae and Dorvilleidae constituted more
than 80% of total polychaete abundance (excluding pro-
todrilid and Osedax polychaetes) on the 2.5-year-old carcasses and more than 70% of total polychaetes on 3.5year carcasses. Osedax japonicus Fujikura et al. 2006 was
Marine Ecology 28 (2007) 219–232 ª 2007 The Authors. Journal compilation ª 2007 Blackwell Publishing Ltd
225
Sperm whale-fall ecosystems in Japan Fujiwara, Kawato, Yamamoto, Yamanaka, Sato-Okoshi, Noda, Tsuchida, Komai, Cubelio, Sasaki, Jacobsen, Kubokawa, Fujikura, Maruyama, Furushima, Okoshi, Miyake, Miyazaki, Nogi, Yatabe & Okutani
(a)
(b)
(c)
(d)
(e)
(g)
(f)
(f)
Fig. 4. Remarkable benthic fauna at the
sperm whale site. (a) Adipicola crypta,
(b) Solemya pervernicosa, (c) Tanea
magnifluctuata, (d) an unidentified protodrilid
polychaete, (e) Osedax japonicus,
(f) Asymmetron inferum and (g) Lyrocteis
imperatoris.
found not only on maxillary bones but also in cephalic
soft tissues and blubber at 1.5 years, and many specimens
were discovered on vertebrae and in soft tissues at 2.5
and 3.5 years (Fig. 4e), as reported by Fujikura et al.
(2006).
Crustacean fauna
Numerous cirripeds identified as Heteralepas sp. were
observed clinging to the nylon nets wrapped around the
whales but not on rocks and sediments far from the
whale carcasses. The total number of crustacean taxa
recorded was similar at 1.5 and 2.5 years, but threefold
greater at 3.5 years (Table 4). Three specimens of the Japanese spider crab Macrocheira kaempferi (Temminck,
226
1836) were only found at the no. 12 whale site at
2.5 years (Fig. 2b).
Other main taxa
The remaining taxa recorded around the whale falls are
listed in Table 5. The total number of taxonomic groups/
species gradually increased from 1.5- to 3.5-year-old carcasses. A new species of lancelet, Asymmetron inferum
Nishikawa 2004, was discovered in the sediments beneath
the whale carcasses at 1.5 years, and was present throughout the 3-year observation period (Fig. 4f). An undescribed sipunculan species was observed in bones and in
sediments underneath the bones in all three years. An undescribed entoproct was originally found in our aquarium
Marine Ecology 28 (2007) 219–232 ª 2007 The Authors. Journal compilation ª 2007 Blackwell Publishing Ltd
Fujiwara, Kawato, Yamamoto, Yamanaka, Sato-Okoshi, Noda, Tsuchida, Komai, Cubelio, Sasaki, Jacobsen, Kubokawa, Fujikura, Maruyama, Furushima, Okoshi, Miyake, Miyazaki, Nogi, Yatabe & Okutani
Sperm whale-fall ecosystems in Japan
Shell length of whale-fall mussels
The shell lengths of the collected whale-fall mussels
A. crypta and A. pacifica were measured (Fig. 6). The two
Adipicola species showed different trends in shell length.
The mean size of A. pacifica was the largest on 1.5-yearold carcasses and gradually decreased thereafter. On the
other hand, that of A. crypta was the smallest on 1.5year-old carcasses and gradually increased. The average
shell length of A. crypta was 1.8-fold larger than that of
A. pacifica on 1.5-year-old carcasses and 5.5-fold larger
on 3.5-year-old ones.
Density and biomass of Adipicola pacifica
The density of A. pacifica was the greatest on 2.5-year-old
carcasses (July 2004) and the total number of the individuals was more than 100,000 per m2 (Fig. 7a). The biomass of A. pacifica was the greatest on 1.5-year-old
carcasses (July 2003), exceeding 17 kgÆm)2, and gradually
decreased during the subsequent two years (Fig. 7b). The
biomass on the surface of 1.5-year-old carcasses was more
than 20-fold greater than that on 3.5-year-old ones.
Sulfide concentrations in sediments beneath whale bones
on land with two whale bones collected in July 2004.
Many individuals of that entoproct were found on the
aquarium glass and on shells of living A. pacifica. One
specimen of the entoproct was also found in an aquarium
onboard during the ROV cruise at 3.5 years. Molecular
phylogenetic analysis of the species showed a close relationship to the genus Loxosomella (Fujiwara et al., unpublished data). More than 10 specimens of the benthic
ctenophore Lyrocteis imperatoris Komai 1941 were discovered around the whale carcasses in July–August 2005
(Fig. 4g). Lyrocteis imperatoris specimens varied substantially in color (yellow, brown, white, white with red
stripes and white with red spots). The tentacles were
occasionally extended (Fig. 4g). Two species of rockfish,
Sebastiscus tertius (Basukov & Chen, 1978) and Helicolenus hilgendorfi (Steindachner and Döderlein, 1884), were
the most abundant fish inhabiting areas around the whale
bones during the 3-year observation period. Several large
specimens of the temperate bass Niphon spinosus Cuvier,
1828 were observed between whale bones in July 2004
and July–August 2005. Other predatory fish, i.e., a conger
eel, a morid cod and an ophidiid cuskeel, were only seen
on 3.5-year-old carcasses.
Vertical profiles of sulfide concentrations were measured
in sediments beneath the whale skeletons during the
3-year observation period (Fig. 8). After 1.5 years, the
highest sulfide concentrations were 0.87 mmÆS2)Ækg)1 at
40
Adipicola crypta
Adipicola pacifica
n=74
n=22
30
Shell Length (mm)
Fig. 5. An ulna of a sperm whale. Adipicola pacifica (circled) was
attached to part of the bone exposed to seawater and Adipicola crypta (squared) was attached to that buried in the sediments. The solid
line indicates the boundary between the two areas.
n=51
20
n=472
10
n=1270
n=152
0
2003
2004
2005
Fig. 6. Mean shell lengths of Adipicola pacifica (solid circles) and
Adipicola crypta (solid squares). Numbers of specimens used for measurements are indicated. Means ± 1 standard error are given.
Marine Ecology 28 (2007) 219–232 ª 2007 The Authors. Journal compilation ª 2007 Blackwell Publishing Ltd
227
Sperm whale-fall ecosystems in Japan Fujiwara, Kawato, Yamamoto, Yamanaka, Sato-Okoshi, Noda, Tsuchida, Komai, Cubelio, Sasaki, Jacobsen, Kubokawa, Fujikura, Maruyama, Furushima, Okoshi, Miyake, Miyazaki, Nogi, Yatabe & Okutani
concentrations of 41.7 mmÆS2)Ækg)1 occurred at 14 cm
below the sediment surface.
Number of individuals/m2
(a) 140,000
120,000
100,000
Discussion
80,000
60,000
40,000
20,000
0
(b)
2003
2005
2004
35
Wet weight (kg/m2)
30
25
20
15
10
5
0
2003
2004
2005
Fig. 7. Time series of density and biomass of Adipicola pacifica
inhabiting surfaces of whale skeletons. (a) Number of individuals per
square meter. (b) Wet weight (kg) of A. pacifica per square meter.
Means ± 1 standard error are given.
2-
AVS (mM S )
0
0
10
20
30
40
50
5
2003
10
2004
2005
15
20
25
Fig. 8. Concentrations of acid-volatile sulfide (AVS) in sediments
beneath the whale carcasses. The ordinate indicates sampling depth
(cm) below the surface of sediments and the abscissa the concentration of AVS (mmÆS2)Ækg)1). Solid triangles show the values sampled in
July 2003, solid circles those in July 2004 and solid squares those in
July 2005.
5 cm below the surface of the sediment. After 2.5 years,
the highest concentrations were 40.5 mmÆS2)Ækg)1 at 8 cm
below the sediment surface. At 3.5 years maximum sulfide
228
To the best of our knowledge, this is the first reported
whale-fall ecosystem on sperm–whale carcasses, providing
new insights into poorly known, shallow-water whale-fall
communities. A sperm whale carcass can sustain a whalefall-specific biological assemblage for more than 3 years,
as has been reported for baleen whales in the deep sea
(Smith & Baco 2003). The invertebrate fauna was similar
to those in other whale-fall communities at the family
level, but not at the species level (Table 6). Mytilid mussels, cocculinid limpets, and dorvilleid and Osedax polychaetes were the most abundant taxa, as in other whalefall communities. However, none of the species in this
study was recorded at any other whale-fall site except for
A. pacifica (Smith & Baco 2003), perhaps because of the
difference in water depth. Molecular phylogenetic analysis
showed that Osedax polychaetes were divided into two
groups based on habitat depth, independent of geographic
location (Fujikura et al. 2006; Fujiwara et al., unpublished
data). In addition, no species conspecific to those at the
whale falls off Cape Nomamisaki appeared at the whale
fall on the Torishima Seamount (depth ¼4037 m), which
was the nearest previously reported whale-fall location
(Naganuma et al. 1996). Further studies of shallow-water
whale falls are required to clarify the influence of water
depth and geography on the distribution of whale-fall
specialists.
Smith & Baco (2003) divided the succession of whalefall communities into four stages, i.e., the ‘mobile-scavenger’, ‘enrichment opportunist’, ‘sulphophilic’ and ‘reef’
stages. The sperm whale-fall communities in this study
were already at the sulphophilic stage in July 2003
(within 1.5 years of reaching the seafloor). Three abundant bivalves, A. pacifica, A. crypta and S. pervernicosa,
harbored thioautotrophic symbionts in their gills
(Fujiwara et al., unpublished data). Adipicola pacifica, in
particular,
attained
extraordinary
abundances
(>100,000 m)2) and biomass (17 kgÆm)2 wet weight);
the biomass of A. pacifica at 1.5 years overlaps the extraordinary biomasses of bivalves observed at hydrothermal
vents and cold seeps (Gebruk et al. 2000). Smith & Baco
(2003) mentioned that the sulphophilic stage might be
markedly long-lasting for large whale skeletons. Schuller
et al. (2004) suggested that the whale-fall reducing habitat was extremely long-lived and able to support life for
many decades, perhaps nearing a century. However, the
sperm whale falls in the present study showed rapid ecological succession of epifauna, although the sperm
whales investigated here were relatively large; the estima-
Marine Ecology 28 (2007) 219–232 ª 2007 The Authors. Journal compilation ª 2007 Blackwell Publishing Ltd
Fujiwara, Kawato, Yamamoto, Yamanaka, Sato-Okoshi, Noda, Tsuchida, Komai, Cubelio, Sasaki, Jacobsen, Kubokawa, Fujikura, Maruyama, Furu-
Nishikawa (2004)
Bennett et al. (1994) Goffredi et al. (2004)
Rouse et al. (2004) Fujikura et al. (2006)
Smith et al. (1998)
Their known habitat and their counterparts reported off California are shown. nr: taxa not reported.
discovered first off Cape Nomamisaki
discovered first off Cape Nomamisaki
nr
nr
nr
Ophryotrocha spp., Dorvillea sp. Dorvilleid sp.
Osedax frankpressi Osedax rubiplumus
Golfingia nicolasi
nr
nr
Protodrilidae gen. sp.
Nereididae gen. sp.
Capitellidae gen. sp.
Dorvilleidae gen. sp.
Osedax japonica
unidentified sp.
Heteralepas sp.
Asymmetron inferum
Ceratostoma inornata
Sperm whale-fall ecosystems in Japan
Polychaeta
Protodrilidae
Nereididae
Capitellidae
Dorvilleidae
Siboglinidae
Sipuncula
Thecostraca
Cephalochordata
Okutani (2000)
nr
McLean (1992)
Okutani (2000)
Cocculina craigsmithi
nr
North-East Japan Sea, South-East of Honshu
and Hokkaido,
attached on sunken wood, 100–200 m deep
Japan, Korean Peninsula, intertidal
rocky bottom to 20 m deep
Muricidae
Adipicola crypta
Solemya pervernicosa
Solemyidae
Gastropoda
Cocculinidae
Skeneidae
Cocculina sp.
Dillwynella vitrea
Okutani (2000) Okutani et al. (2003)
Okutani (2000)
nr
Smith et al. (1989), Okutani (2000) Okutani et al. (2003)
Idas washingtonia
South-East of Honshu, North-East Japan Sea, Hawaii,
attached on sunken whale bones, 150–715 m deep
South-East of Honshu, Hawaii, 100–200 m deep
South-East of Honshu and Hokkaido, 100–1500 m deep
Adipicola pacifica
Bivalvia
Mytilidae
known habitat
off Nomamisaki
taxa
Table 6. Abundant taxa collected at the whale-fall site off Cape Nomamisaki.
counterpart reported off California
reference
shima, Okoshi, Miyake, Miyazaki, Nogi, Yatabe & Okutani
ted body weight of the smallest specimen was 22 t and
that of the largest 39 t.
The diversity and structure of the epifaunal communities changed markedly from the sulphophilic to the beginning of the reef stages between July 2003 and July 2004, at
least on the surfaces of the whale skeletons. The biomass
of A. pacifica was the greatest on the 1.5-year-old carcasses
and rapidly decreased thereafter. Suspension feeders such
as crinoids, basket stars, cnidarians and a benthic ctenophore were recorded on 2.5- and/or 3.5-year-old carcasses,
which should be an indication of the reef stage. These taxa
were not observed to attach to regions where bacterial
mats, A. pacifica or O. japonicus appeared. These suspension feeders might be intolerant of reduced chemicals and/
or organic compound effluents from whale skeletons.
Indeed, many suspension feeders already existed on the
concrete sinkers in 2003. In addition, carnivorous
gastropods and predatory fish were abundant around 2.5and 3.5-year-old carcasses. The reason for such rapid succession was unclear, but one possibility was that the biological decomposition, including bacterial degradation could
be faster with the higher water temperature at these sperm
whale-fall sites (12 C) than at the 4 C sites studied in
the deep sea by Smith & Baco (2003). Shallow-water whale
falls have rarely been reported, and rapid succession on
shallow whale falls may explain their apparent rarity.
Another possible cause for more rapid succession in our
study might be the difference in whale species (sperm versus baleen whales) between the shallow- and deep-water
studies. A new sperm whale carcass discovered at a deeper
water depth (925 m) off Japan in January 2006 provides
an opportunity to determine whether sperm whale-fall
communities generally show rapid succession.
Compared to the rapid epifaunal succession, the diversity of infauna was relatively stable throughout the 3-year
observations, i.e., A. crypta, S. pervernicosa, and A. inferum
were abundant in each year. Sulfide concentrations in the
sediments appeared to be sufficient for sulphophilic infauna at all sampling times, especially at 2.5 and 3.5 years
(Fig. 8) (cf. Smith & Baco 2003). Further investigation
will clarify whether the infaunal succession of shallowwater whale falls is rapid as well, compared with deep-sea
whale falls.
Adipicola pacifica and A. crypta showed different trends
in shell length in the present study, which implied a difference in the habitat conditions between epi- and
infauna. Mean Adipicola pacifica size became shorter each
year, indicating that its life span was less than 1 year and
the conditions of its habitat had worsened. Consequently,
new generations apparently did not grow as fast as the
earlier generations. The whale bones collected in 2005
were very fragile and porous, and core samples collected
from vertebrae were less oily and malodorous than those
Marine Ecology 28 (2007) 219–232 ª 2007 The Authors. Journal compilation ª 2007 Blackwell Publishing Ltd
229
Sperm whale-fall ecosystems in Japan Fujiwara, Kawato, Yamamoto, Yamanaka, Sato-Okoshi, Noda, Tsuchida, Komai, Cubelio, Sasaki, Jacobsen, Kubokawa, Fujikura, Maruyama, Furushima, Okoshi, Miyake, Miyazaki, Nogi, Yatabe & Okutani
collected during the first and second cruises, which
implied that many organic compounds such as energyrich lipids and proteins had disappeared. Meanwhile,
Adipicola crypta became larger with time. It appeared to
have a longer life than A. pacifica and to survive for more
than 3 years. Several specimens of A. crypta have been living with whale bones in our aquaria since July 2004, few
dead shells have been found in the tanks, and the number
of living specimens has remained stable. Adipicola crypta
lived in the sediments beneath whale carcasses, in which
the sulfide concentrations were higher in July 2004 and
July 2005 than in July 2003. Energy-rich organic compounds apparently oozed from the whale bones into the
sediments, and a suitable reducing environment for infaunal species might have formed through anaerobic bacterial degradation of the compounds just beneath the whale
carcasses.
Decomposition of the largest whale carcass (whale no. 6)
seemed to be slower than that of the others at the beginning
of this study. However, the benthic communities were similar among the carcasses observed, although the body sizes
of the whales were not homogeneous. The differences in
the sizes of the whales in this study might not be a significant influence on benthic fauna at this stage of whale-fall
development.
A shallow-water chemosynthetic community has been
reported in Kagoshima Bay at 80 m (Hashimoto et al.
1993), which was close to the sperm whale site (Fig. 1).
The vestimentiferan tubeworm Lamellibrachia satsuma
was the most abundant species in the bay (Miura et al.
1997) and, based on molecular phylogenetic analyses, the
same species was recorded at hydrothermal vents on the
Nikko Seamount (470 m) 1500 km south of both Kagoshima Bay and the sperm whale site (Kojima et al. 2001).
The whale-fall site off Cape Nomamisaki was thought to
be a good candidate for a new distribution site of L. satsuma because it was in both the geographic and water
depth ranges of the tubeworm. However, no vestimentiferans (including L. satsuma) were found at the whale-fall
site. In addition, no vesicomyid clams, no Bathymodiolus
mussels and no chemosymbiotic gastropods were recorded at this site, which implies low species-level similarity
between this shallow-water whale-fall and deep-sea vent/
seep environments. It is possible that a suitable chemosynthetic environment for tubeworms and other chemosymbiotic taxa would be generated after 3.5 years at the
Cape Nomamisaki whale falls.
The new species of lancelet A. inferum was discovered
in the sperm whale-fall habitats; this was the first recorded cephalochordate from a chemosynthetic habitat and
the deepest recorded branchiostoma (Nishikawa 2004).
In general, lancelets inhabit shallow, subtidal tropical,
subtropical and temperate sand flats. They prefer coarse
230
sand with fairly fast water flow and do not inhabit silty
sediments (Berrill 1987; Nishikawa et al. 1997). However,
this whale fall-related lancelet preferred a deeper, reducing, organic compound-rich environment. Physiological
experiments will clarify the mechanism of adaptation of
this species to such an extreme environment.
The benthic ctenophore L. imperatoris was described as a
new species in 1941 (Komai 1941) and has not been reported for more than 60 years. The type specimens were collected in a dredge survey. Therefore, this was the first
scientific observation of L. imperatoris in situ. It is not certain, however, whether this benthic ctenophore is specifically a whale fall-related species because many specimens
appearing around the skeletons did not attach to the bones.
The naticid gastropod T. magnifluctuata is also a very
rare species. The only two reports of this species (Kuroda
1961; Matsumoto 1979) did not describe the habitats, soft
tissues and operculum. This species is assumed to be carnivorous but its diet was not clarified.
The Osedax species collected in this study was examined
morphologically and phylogenetically and was described as
the new species O. japonicus (Fujikura et al. 2006). The
most characteristic feature of its ecology was the whale-fall
habitat. Unlike other known Osedax species, Osedax japonicus appeared upon cephalic soft tissues and blubber in
addition to whale skeletons. It was unclear whether its
habitation on the soft tissues was due to the whale species,
the Osedax species or both. One possible explanation
could be that the large amount of lipids in sperm whales
supports Osedax growth. Further sperm whale-fall studies
in Sagami Bay may resolve this question.
Shallow-water whale falls appear to be rarely encountered, possibly because they are easily decomposed by biological/microbiological activities at relatively higher water
temperatures and/or they are quickly buried in sediments
transported from shore. Therefore, a large number of
whale-fall dependent species may remain undiscovered.
Molecular phylogenetic analyses indicated that A. pacifica
diverged prior to other bathymodiolin mussels (Miyazaki
et al., personal communication), Osedax is a sister taxon
to hydrothermal vent/seep siboglinids (Rouse et al. 2004;
Glover et al. 2005; Fujikura et al. 2006), A. inferum
diverged early in the evolution of lancelet (Kon et al.
2005) and L. imperatoris occupies a basal position among
ctenophores (Fujiwara et al., unpublished data). Shallowwater whale-fall ecosystems might have thus played an
important role in the evolution not only of deep-sea
chemosynthetic ecosystems but also of all marine life.
Summary
Sperm whale-fall communities were investigated for
3 years using an ROV. Five sperm whale carcasses sus-
Marine Ecology 28 (2007) 219–232 ª 2007 The Authors. Journal compilation ª 2007 Blackwell Publishing Ltd
Fujiwara, Kawato, Yamamoto, Yamanaka, Sato-Okoshi, Noda, Tsuchida, Komai, Cubelio, Sasaki, Jacobsen, Kubokawa, Fujikura, Maruyama, Furushima, Okoshi, Miyake, Miyazaki, Nogi, Yatabe & Okutani
tained chemosynthesis-based communities at depths of
219–254 m, which were similar to the deeper whale-fall
communities in general but with certain unique features.
The rate of epifaunal succession was notably more rapid
than that of deeper communities on large whale falls. The
sulphophilic stage appears to be much shorter, although
the whale carcass sizes should have been sufficiently large
for long-term support of sulphophilic species. No vent/
seep specialists were present at this whale-fall site and
many new, poorly described and/or rarely encountered
species appeared. Further information on whale carcasses
from a wide range of areas and depths will clarify the spatiotemporal dynamics of deep-sea life in such isolated,
ephemeral habitats.
Acknowledgements
We wish to express our sincere thanks to Professor Hidehiro Kato (Tokyo University of Marine Science & Technology) and local inhabitants for their efforts in dropping
the whale carcasses. We are very grateful for helpful comments from Drs Hiroshi Senou (Kanagawa Prefectural
Museum of Natural History) and Keiichi Matsuura (The
National Science Museum) on the identification of fish,
to Professor Toshiyuki Yamaguchi (Chiba University) on
the identification of the cirriped and to Dr Tohru Iseto
(The Kyoto University Museum) and Professor Yoshihisa
Shirayama (Seto Marine Biological Laboratory, Kyoto
University) on the identification of the entoproct. We are
deeply obligated to Prof. Craig Smith (associate editor) and
all three reviewers for their careful and considerate review
as they have indeed helped us improve this manuscript. We
thank Dr Dhugal J. Lindsay for his useful suggestions and
Mr Mamoru Sano for creating maps. We thank Mr Hitoshi
Tanaka, Ms Misumi Aoki, and Mr Kaoru Tsukuda for
active support aboard, Ms Kazuyo Okano for groundwork
for the first cruise, Dr Yukiko Fujii, Ms Yoko Sasaki and
Ms Hiroko Nakamura (JAMSTEC) for laboratory assistance
and Ms Shizue Kanai and Ms Tomomi Nagashima (JAMSTEC) for administrative help. We also thank the operation
teams of the ROV Hyper-Dolphin and the JAMSTEC
deep tow systems and the captains and crew of the R/V
Natsushima and R/V Kaiyo.
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