Jelly-falls historic and recent observations: A review to drive future research directions

Abstract

The biological pump describes the trans-port of particulate matter from the sea surface to the ocean's interior including the seabed. The contribution by gelatinous zooplankton bodies as particulate organic matter (POM) vectors (''jelly-falls'') has been neglected owing to technical and spatiotemporal sampling limitations. Here, we assess the existing evidence on jelly-falls from early ocean observations to present times. The seasonality of jelly-falls indi-cates that they mostly occur after periods of strong upwelling and/or spring blooms in temperate/subpolar zones and during late spring/early summer. A con-ceptual model helps to define a jelly-fall based on empirical and field observations of biogeochemical and ecological processes. We then compile and discuss existing strategic and observational oceano-graphic techniques that could be implemented to further jelly-falls research. Seabed video-and pho-tography-based studies deliver the best results, and the correct use of fishing techniques, such as trawling, could provide comprehensive regional datasets. We conclude by considering the possibility of increased gelatinous biomasses in the future ocean induced by Guest editors: J. E. Purcell, H. Mianzan & J. R. Frost / Jellyfish Blooms: Interactions with Humans and Fisheries

Full text

JELLYFISH BLOOMS Review Paper
Jelly-falls historic and recent observations: a review to drive
future research directions
Mario Lebrato •Kylie A. Pitt •Andrew K. Sweetman •Daniel O. B. Jones •
Joan E. Cartes •Andreas Oschlies •Robert H. Condon •Juan Carlos Molinero •
Laetitia Adler •Christian Gaillard •Domingo Lloris •David S. M. Billett
!Springer Science+Business Media B.V. 2012
Abstract The biological pump describes the trans-
port of particulate matter from the sea surface to the
ocean’s interior including the seabed. The contribution
by gelatinous zooplankton bodies as particulate
organic matter (POM) vectors (‘‘jelly-falls’’) has been
neglected owing to technical and spatiotemporal
sampling limitations. Here, we assess the existing
evidence on jelly-falls from early ocean observations
to present times. The seasonality of jelly-falls indi-
cates that they mostly occur after periods of strong
upwelling and/or spring blooms in temperate/subpolar
zones and during late spring/early summer. A con-
ceptual model helps to define a jelly-fall based on
empirical and field observations of biogeochemical
and ecological processes. We then compile and
discuss existing strategic and observational oceano-
graphic techniques that could be implemented to
further jelly-falls research. Seabed video- and pho-
tography-based studies deliver the best results, and the
correct use of fishing techniques, such as trawling,
could provide comprehensive regional datasets. We
conclude by considering the possibility of increased
gelatinous biomasses in the future ocean induced by
Guest editors: J. E. Purcell, H. Mianzan & J. R. Frost / Jellyfish
Blooms: Interactions with Humans and Fisheries
M. Lebrato (&)!A. Oschlies !J. C. Molinero
GEOMAR, Helmholtz Centre for Ocean Research Kiel,
Du
¨sternbrooker Weg 20, 24105 Kiel, Germany
e-mail: mlebrato@ifm-geomar.de
K. A. Pitt
Australian Rivers Institute, Coast and Estuaries, Griffith
University, Brisbane, QLD 4222, Australia
A. K. Sweetman
Norwegian Institute for Water Research,
Thormøhlensgate 53D, 5006 Bergen, Norway
A. K. Sweetman
Centre for Geobiology, University of Bergen, Bergen,
Norway
D. O. B. Jones !D. S. M. Billett
National Oceanography Centre, European Way,
Southampton SO14 3ZH, UK
J. E. Cartes !D. Lloris
Institut de Cie
`ncies Del Mar de Barcelona, CSIC, Passeig
Marı
´tim de la Barceloneta 37-49, 08003 Barcelona, Spain
R. H. Condon
Dauphin Island Sea Lab, Dauphin Island, AL 36528, USA
L. Adler
Biocenter Grindel and Zoological Museum, Martin-
Luther-King-Platz 3, 20146 Hamburg, Germany
Present Address:
L. Adler
School of Geological Sciences, University College
Dublin, Belfield, Dublin 4, Ireland
C. Gaillard
Universite
´de Lyon 1, UMR CNRS 5125, 2 rue Raphae
¨l
Dubois, 69622 Villeurbanne cedex, France
123
Hydrobiologia
DOI 10.1007/s10750-012-1046-8

upper ocean processes favouring their populations,
thus increasing jelly-POM downward transport. We
suggest that this could provide a ‘‘natural compensa-
tion’’ for predicted losses in pelagic POM with respect
to fuelling benthic ecosystems.
Keywords Biological pump !Gelatinous
zooplankton !Jelly-fall !Organic matter
Introduction: particulate organic matter (POM)
and jelly-falls
The input of POM drives secondary production and
most benthic ecosystem processes in the deep-sea
(Ruhl et al., 2008; Smith et al., 2008). POM inputs
mainly include autochthonous particles from the
euphotic zone, ranging in increasing size from phy-
todetritus (organic-rich material derived from phyto-
plankton blooms) (Beaulieu, 2002; Smith et al., 2008),
marine snow (Caron et al., 1986; Alldredge & Silver,
1988), mucilaginous aggregates (Cartes et al., 2007;
Martin & Miquel, 2010), mucous sheets from zoo-
plankton (Robison et al., 2005; Lombard & Kiorbe
2010), faecal pellets (reviewed by Turner, 2002), wood
particles (Turner, 1973), and macrophyte detritus
(Vetter & Dayton, 1998,1999; Cartes et al., 2010) to
fish and whale carcasses (Soltwedel et al., 2003; Smith
& Baco, 2003; Gooday et al., 2010).
Jelly-falls can be defined as point source organic
matter inputs (as corpses/carcasses) that sink through
the water column (remineralizing as dissolved organic/
inorganic components), eventually causing an accu-
mulation of jelly-POM (J-POM) at the seabed (Fig. 1).
Numerous gelatinous zooplankton groups have been
shown to accumulate at the ocean floor including the
Cnidaria (Scyphozoa) and Thaliacea (Pyrosomida,
Doliolida, and Salpida) (Table 1). The significance
and magnitude of sinking material in the biological
pump are primarily assessed by a variety of indirect
techniques (Buesseler et al., 1992; Jahnke, 1996;
Marchant et al., 1999) that cannot target the J-POM
associated with jelly-falls. They include remote sens-
ing algorithms (Behrenfeld & Falkowski, 1997; Balch
et al., 2007), surface-tethered and neutrally buoyant
sediment traps (Lampitt et al., 2001; Buesseler et al.,
2007), and acoustic backscatter profiling sensors (ABS
and ADCP) to study particles and biomass in the water
column (Merckelbach & Ridderinkhof, 2006; Jiang
et al., 2007). Sediment traps are the most used device,
but they often underestimate the contribution of large
particles and detritus (e.g. Rowe & Staresinic, 1979;
but see Conte et al., 2003; Buesseler et al., 2007).
Jelly-falls can only be sampled directly using tech-
niques such as video (Wiebe et al., 1979; Lebrato &
Jones, 2009), towed/still photography (Roe et al.,
1990; Billett et al., 2006; Sweetman & Chapman,
2011), or benthic trawling (Sartor et al., 2003) (see
Table 2for other techniques/strategies). Therefore,
although many sources of organic material have been
widely studied and POM/DOM remineralization
dynamics considered in biogeochemical models as a
result (e.g. Burd et al., 2010), jelly-falls are relatively
unexplored sources of POM, despite a significant
fraction of the pelagic biomass being sequestered in the
bodies of gelatinous zooplankton.
The study of jelly-falls represents a major challenge
in the understanding of the biological pump mainly
due to technical/sampling hurdles, and although there
is no consensus that the oceans will turn into a ‘‘jelly-
slime’’ ecosystem (e.g. Jackson, 2008), gelatinous
zooplankton biomass appears to be increasing in
certain areas of the world’s oceans (Mills, 2001;
Richardson et al., 2009; Purcell, 2012). As such,
increased gelatinous biomass may translate into
increased transfer of this material to the ocean floor
and thus enhancing the magnitude and importance of
the biogeochemical and ecological processes associ-
ated with jelly-falls. Thus, there is a pressing need for
research on gelatinous zooplankton post-bloom
processes.
Our primary objective is to provide a qualitative
overview of historical and present records of jelly-
falls, as well as the environmental context in which
they were studied. Secondly, we define and concep-
tually model a general jelly-fall within the biological
pump, including a synthesis of the factors triggering
these events. We also assess the seasonality of jelly-
falls from the available data and the benthic organisms
that were observed feeding on the material. Our third
objective is to discuss the possible consequences of
increased gelatinous biomasses in the future ocean and
provide a summary of the observational techniques
and platforms that are, or could be used to study jelly-
falls and their biogeochemical feedbacks.
Hydrobiologia
123

Jelly-fall observations in the field
Thaliaceans
During the 1872–1876 H. M.S. Challenger expeditions,
Moseley (1880) realized the potential importance of
jellyfish in the biological pump by experimentally
assessing the time it took a dead salp to sink 20 cm in a
cylinder (*20 s). He then left the carcass in the
cylinder for 1 month and noticed that it did not
decompose completely. He subsequently wrote: ‘‘the
deep-sea has to derive food for its inhabitants entirely
Fig. 1 Conceptual model
of common processes
beginning with sinking and
the start of remineralization
in the euphotic and twilight
zones to deposition at the
seabed followed by
decomposition and
scavenging. Under
‘‘material arriving at depth
z’’, we have identified five
critical factors that
determine the amount of
material reaching the
seabed. The links to
‘‘bacterioplankton’’ and
‘‘phytoplankton’’ only
proceed in the euphotic/
twilight zone. Jelly-falls are
linked to the ‘‘jelly-pump’’
concept (Condon &
Steinberg, 2008; Condon
et al., 2010) through the
production of J-DOM in the
water column and at the
seabed. J-DOM is organic
matter that fuels other
trophic levels, which can
occur while the organisms
are still alive (e.g. Condon
et al., 2011) or when dead
(Hansson & Norrman, 1995)
Hydrobiologia
123

Table 1 A compilation of naturally occurring jelly-falls
Location Origin Species Material
state
a
Latitude
(range)
b
Longitude
(range)
b
Depth
(m)
c
Survey device Duration
d
Reference
Norwegian Sea
(Atlantic Ocean)
Likely Scyphozoa Pending DNA
analysis
e
Det. 66.14"N 3.94"E 1,380
(8.3/-1)
ROV (video) 7 days (S) Jones et al. (2010)
Norwegian Sea
(Atlantic Ocean)
Scyphozoa P. periphylla F/Dec. 60.40"N–
60.41"N
5.09"E–
5.10"E
396–443
(-/7)
Yo–Yo (towed
camera)
1 day (Spr.) Sweetman &
Chapman (2011)
Japan Sea (Pacific Ocean) Scyphozoa A. limbata F 42.58"N 143.96"E 320
(17/2.2)
ROV (video) Unknown
(S)
Miyake et al. (2002)
Chesapeake Bay
(Atlantic Ocean)
Scyphozoa C. quinquecirrha F 38.59"N 76.12"W 1.5–3
(15/14)
Visual
(observers)
90 days (S) Sexton et al. (2010)
f
Japan Sea (Pacific Ocean) Scyphozoa N. nomurai F 35.8"N–
36.3"N
136"E–
135.5"E
146–354
(22/10)
VTR system
(towed camera)
35 days
(S–A)
Yamamoto et al.
(2008)
Japan Sea (Pacific Ocean) Scyphozoa P. polylobata F 34.91"N 138.65"E 453 (16/8) ROV (video) Unknown
(S)
Miyake et al. (2005)
Santa Catalina Basin
(Pacific Ocean)
Scyphozoa Pelagia sp. Unk. 32.46"N 117.49"W[1,000
(17/4)
Photographs Unknown
(N)
Jumars (1976)
Bermuda (Atlantic Ocean) Scyphozoa Cassiopeia
xamachana
F/Dec./
Det.
32.34"N 64.70"W 3 (25–25) Photographs
(quadrats)
Unknown
(S)
M. Lebrato
(unpublished)
Gulf of Aqaba (Red Sea) Scyphozoa A. aurita F 29.50"N 34.91"E 20
(25–23)
Photographs
(scuba diver)
Unknown
(Sp. #)
Alamaru et al. (2009)
Arabian Sea
(Indian Ocean)
Scyphozoa Probably
C. orsini
F 22.95"N 66.61"E 900
(25/9.5)
WASP (towed
camera)
1 day (S #) Murty et al. (2009)
Arabian Sea
(Indian Ocean)
Scyphozoa C. orsini F/Dec./
Det.
22.58"N–
23.50"N
60.65"E–
59.04"E
304 –
3,299
(25/2)
SHRIMP (towed
camera)
17 days
(W #)
Billett et al. (2006)
Japan Sea (Pacific Ocean) Thaliacean
(Doliolidae)
Not identified F 34.40"N 150"E 150
(16/12)
Sediment trap 5 days
(Sp.)
Takahashi et al.
(2010)
g
Tyrrhenian Sea
(Mediterranean Sea)
Thaliacean
(Pyrosomatidae)
P. atlanticum F/Dec. 42.30"N 10.60"E 300–650
(25/12)
Bottom trawling 1995–1999
(Sp. S)
Sartor et al. (2003)
h
Alboran Sea-Gulf of Lions
(Mediterranean Sea)
Thaliacean
(Pyrosomatidae)
P. atlanticum F/Dec. 36.24"N–
42.39"N
5.20"W–
3.63"W
43–791
(18/13)
Bottom trawling
(GOC 73)
1994–2005
(Sp. #)
Bertrand et al.
(2002), MEDITS-
ES
i
Madeira Abyssal Plain
(Atlantic Ocean)
Thaliacean
(Pyrosomatidae)
P. atlanticum F/Dec. 31.28"N 25.40"W 5,433
(20/2.2)
BATHYSNAP
(fixed camera)
16 days (S) Roe et al. (1990)
Cape Verde
(Atlantic Ocean)
Thaliacean
(Pyrosomatidae)
P. atlanticum F 15.80"N 23.50"W Unknown
(26/-)
Unknown Unknown
(N)
Monniot & Monniot
(1966)
Ivory Coast
(Atlantic Ocean)
Thaliacean
(Pyrosomatidae)
P. atlanticum F/Dec. 5.15"N-
4.94"N
4.51"W-
4.49"W
26–1,275
(25/4)
ROV (video) 60 days
(W #)
Lebrato & Jones
(2009)
Hydrobiologia
123

Table 1 continued
Location Origin Species Material
state
a
Latitude
(range)
b
Longitude
(range)
b
Depth (m)
c
Survey device Duration
d
Reference
Cook Strait
(Pacific Ocean)
Thaliacean
(Pyrosomatidae)
P. atlanticum Dec. 41.73"S 174.3"E 100 (15/9) Bottom trawling Unknown
(Sp.)
Hurley & McKnight
(1959)
Tasman Sea
(Pacific Ocean)
Thaliacean
(Pyrosomatidae)
P. atlanticum Unk. 42"S 148"E 330–640
(14/7)
Stomach content Unknown
(W)
Cowper (1960)
Gulf of Alaska
(Pacific Ocean)
Thaliacean
(Salpidae)
S. fusiformis F 58.33"N 136.83"W 1–10 (7/4) Visual
(scuba diver)
120 days
(Sp.)
Duggins (1981)
Sargasso Sea
(Atlantic Ocean)
Thaliacean
(Salpidae)
S. aspera F/Dec. 38.60"N–
39"N
71.4"E–
71.1"E
2,500–3,000
(19/3)
ROV (video) 4 days (S) Cacchione et al.
(1978)
Sargasso Sea
(Atlantic Ocean)
Thaliacean
(Salpidae)
S. aspera F/Dec. 38"N–
40"N
72.5"E–
70"E
2,000–3,000
(19/3)
ROV (video) 30 days (S) Wiebe et al. (1979)
Gulf of Aqaba
(Red Sea)
Thaliacean
(Salpidae)
Not
identified
F 34.90"N 29.50"E 20 (25/23) Photographs
(scuba diver)
Unknown
(Sp. #)
Alamaru et al.
(unpublished)
j
a
Material state refers to the condition in which the material was found: Dec. decomposing, Det. detritus, Ffresh, unk. unknown (if not stated)
b
Range for latitude, longitude and depth indicates that in some cases the material was retrieved along a gradient of depths and not in isolation (see reference paper for additional
information)
c
In situ surface and BT ("C) are included in parentheses when available in the original study or otherwise compiled from the GLODAP database (Key et al., 2004) and the World
Ocean Atlas (http://odv.awi.de/en/data/ocean) in the nearest place available at the same depth
d
Duration only indicates the time that the material was observed or surveyed at the seabed and does not indicate annual events; otherwise the time-series is given for annual
depositions. The season is indicated as: Nnot available; Sp. spring, Ssummer, Aautumn, Wwinter. # indicated when the event happened after seasonal upwelling and/or monsoon
winds (e.g. tropical latitudes or specific cases like the Mediterranean Sea)
e
Jelly material was unidentifiable to species level. Bar-coding with mtDNA and 18S rDNA ITS regions in progress to determine the affiliation
f
The authors do not show seabed evidence. The potential POC flux to the sediments was relatively small (12.5–72.5 mg C m
-2
year
-1
) in comparison with the total annual flux
to the sediments in the area (61.2 g C m
-2
year
-1
Kemp et al., 1997)
g
Carcasses recorded in sediment traps (export flux =1.05 mg C m
-2
day
-1
, sinking speed =4,000 m day
-1
, small degradation observed)
h
The data used for P. atlanticum correspond to the trawling catch from the seabed. The carcasses were dead at the seabed and decomposing
i
The data were in the MEDITS-ES project (International bottom trawl survey in the Mediterranean) (http://www.sibm.it/SITO%20MEDITS/). The data for P. atlanticum
correspond to the trawling catch from the seabed
j
A. Alamaru also reports on the presence of salps at the seabed in the same area as A. aurita
Hydrobiologia
123

Table 2 Sampling techniques and initiatives that may be available to monitor jelly-falls
Study method Description Advantages Disadvantages
Large scale (regional)
(1) Deep ocean observatories
network (e.g. EUR-
OCEANS, OceanSITES,
ESONET) and offshore
scientific platforms (e.g.
PLOCAN)
Long-term reference network
stations could be used to
monitor seabed processes
associated with jelly-falls.
They could be used to study
the organisms and carcasses
in the water column and their
arrival at the seabed by use of
camera arrays. Global
distribution
The moorings and cruises are in
place so it is a matter of
adapting the strategy. Could
have camera systems
throughout the year with
periodic recoveries. In situ
and real time monitoring
Challenging to study the jellies
in the water column with
camera devices. Possibility
that jelly-falls do not occur
near the stations and/or the
seabed may too deep for jelly-
falls to be observed)
(2) Collaborations with
industry (e.g. SERPENT
project and similar)
The offshore oil and gas
industry has regular access to
expensive equipment (e.g.
ROVs, camera systems) used
in monitoring their own
infrastructures. This
equipment is not routinely
used in scientific studies, but
through collaboration it could
be used to study jelly-falls at
specific times of the year
Access to state-of-the-art
expensive equipment to study
the seabed in deep waters.
ROVs used in industry
operations follow paths,
allowing transect study. They
cover a larger seabed area
than normal in a scientific
study
Obtaining agreements with key
industry personnel with
access to the facilities.
Confidentially and data
release may take time to
arrange. Surveys are confined
to where the infrastructure
exists. Cannot deviate greatly
from established survey lines
Medium scale (local)
(3) Scientific ROV surveys Used at known sites of jelly-
falls to monitor the
depositions in transects
Real-time monitoring and
quantitative or qualitative
data available at the seabed
Time available to conduct the
survey. Total area covered.
Exclude water column
processes. Expensive
(4) Towed and drop cameras
from a vessel
Either used at known sites of
jelly-falls or use to search for
depositions in transects/
specific locations
Real-time monitoring and
quantitative or qualitative
data available at the seabed.
Can cover a relatively large
area
Time available to conduct the
survey. Camera angle of view
much less than ROV camera.
Exclude water column
processes
(5) Time-lapse cameras (e.g.
BATHYSNAP and benthic
landers)
Used at known sites of jelly-
falls to study the evolution of
the material over time. A
network of time-lapse
cameras also feasible at
specific locations
Real-time monitoring and
qualitative data available at
the seabed. Time component
of the jelly-falls
Limited area covered. No
biomass data. Jelly-fall may
not occur where cameras are
installed. Camera angle of
view restricted. Exclude
water column processes
(6) Trawling (from fisheries) The fishery industry and other
commercial species surveys
(e.g. MEDITS) have records
of bycatch organisms trawled
at the seabed, including jelly-
falls (carcasses)
Quantitative or qualitative data
available at the seabed. Large
areas covered over
bathymetric gradients. Time
component often available
Obtaining agreements with
industry personnel that have
access to the facility. Surveys
confined to the industry study
of commercial species.
Excludes water column
processes. Environmentally
destructive
(7) Acoustic/electronic
tagging studies
Living individuals in large
blooms could be acoustically/
electronically tagged to
follow their fate
Real-time study of individuals
in a jelly-fall. Time
component of sinking and
deposition
Difficulty of tag attachment to
gelatinous body. Premature
release of the tag. Limited
information
Hydrobiologia
123

from debris of animals and plants falling to the bottom
from the water above them. The dead pelagic animals
must fall as a constant rain of food. It might be
supposed that the animal carcasses would consume so
long a time in dropping to the seabed that their soft
tissues would be decomposed’’ (Mosely 1892). This is,
to the best of our knowledge, the first mention of jelly-
falls in the literature. A number of both quantitative
and qualitative studies have followed since then
(Table 1), but they still remain scarce when compared
with studies that have assessed the importance of other
POM vectors (Turner, 2002).
Hurley & McKnight (1959) were the first to report
on a natural jelly-fall when they found the thaliacean
Pyrosoma atlanticum Peron 1804 on the seabed off
New Zealand. The organisms were sampled with a
bottom trawl between 160- and 170-m depth (bottom
temperature (BT) =9"C) during spring and were
described as ‘‘resting’’ on the seabed. Their observa-
tions are further supported by reports from the same
area of seabed being covered in P. atlanticum
carcasses in 1952 (H. B. Fell pers. obs. reported
to Hurley & McKnight, 1959) and reports that
local fishermen frequently trapped large quantities of
moribund carcasses at certain times of the year.
Similar fishermen’s reports occur in the Mediterranean
Sea (e.g. Sartor et al., 2003). Later, in the Tasman Sea,
Cowper (1960) found that the stomachs of freshly
caught carangid fish were full of P. atlanticum
carcasses during winter. All fish were caught close to
the bottom (BT =7"C); therefore, the authors con-
cluded that they were feeding either on recently settled
carcasses or on moribund individuals on or near the
seabed. A further analysis of stomach contents from
the same fish species in the Tasman Sea from January
to October revealed that the carcasses were most
abundant in stomachs in January and March (Cowper,
1960). There are other observations in New South
Wales, Australia of the giant pyrosomid Pyrosoma
spinosum Herdman 1888 near to or deposited on rocky
bottoms, and also portions of salps being recovered
from stomachs of carangid fish feeding at the seabed
(Griffin & Yaldwyn, 1970).
A considerable number of more recent studies
document pyrosome falls. In the tropical Atlantic (off
Cape Verde), Monniot & Monniot (1966) recorded
moribund P. atlanticum at the seabed. In the deep
Atlantic Madeira Abyssal Plain, high densities of
pyrosomids were observed in the first 800 m of the
water column (Roe et al., 1990). A survey using a fixed
camera photographed a single carcass in an advanced
state of decomposition at 5,433-m depth (BT =2.2"C).
Table 2 continued
Study method Description Advantages Disadvantages
Small scale (local)
(8) Large sediment traps
(?5 m)
If a neutrally buoyant sediment
trap is developed to follow
blooms it may deliver data on
the associated sinking
material
Quantitative data in the water
column. Possible to combine
with a method at the seabed
Probably unable to catch much
of the sinking jelly-fall.
Problems with organisms that
vertically migrate and are
mistakenly trapped alive.
Cost-effective problems
(9) Moored and free-drifting
profilers
Some in development to
measure water column
properties over time (McLane
labs, SeaCycler). If installed
with a camera, study could
cover the entire water column
to the seabed
Possible to monitor entire water
problem over time.
Quantitative data. Possible to
relate camera data and water
column properties
Camera installation problems.
Jelly-fall may not occur
where the profilers are
installed. Sinking speed of
carcasses not tracked by
profiler
(10) Genetic tools in
sediments
Sediment proxy on freshly
deposited gelatinous material
can be tested using mtDNA
and nuclear DNA
Possible to obtain a
identification (general or
specific) from jelly-falls in
the sediment depending on
the decomposition time.
Possible to combine with
camera studies if material is
visible. Time component may
be available
Limited to very fresh
depositions. DNA
contamination problems.
Limited area covered
Hydrobiologia
123

A starfish and a crustacean scavenged the carcass, which
took [16 days to decompose completely. Recently,
Lebrato & Jones (2009) reported a vast jelly-fall of
P. atlanticum off the Ivory Coast, West Africa during
ROV (remotely operated vehicle) surveys. Decompos-
ing carcasses formed large patches (*1–20 m
2
) and
accumulated in troughsand channels (to a thickness of at
least 0.5 m) from the shelf (\200 m) to the deep slope
([1,200 m) (BT =4"C). The organic carbon contribu-
tion was estimated to be more than 20 g C m
-1
in some
areas, which is almost ten times the annual fluxes in the
area, as measured by sediment traps (Wefer & Fischer,
1993). Carcasses were very abundant (707 individuals
100 m
-2
) at the maximum depth surveyed (1,275 m)
and the maximum depth of the deposit could not be
determined. Megafauna (including echinoderms and
crustaceans) were observed 63 times directly feeding on
the material (Lebrato & Jones, 2009). In the Mediter-
ranean Sea (Alboran Sea to the Catalan Sea), jelly-falls
of P. atlanticum were identified and sampled from 1994
to 2005 (spring and summer) during bottom trawling
down to 800 m (average BT =13"C) in the MEDITS-
ES surveys (Bertrand et al., 2002) (Fig. 2B). The catch
often exceeded 300 carcasses per haul. This dataset
provided the first evidence of jelly-falls encompassing
entire continental margins during a period of 12 years
(Fig. 2B). Living P. atlanticum were recovered from
benthic trawls in canyon heads and walls (Cartes et al.,
2009) near the wind-driven upwelling region of the Gulf
of Lions (Johns et al., 1992). Sartor et al. (2003) reported
catches in benthic trawls from 1995 to 1999 in the
Mediterranean Sea (Tyrrhenian Sea) with numerous
P. atlanticum occurring at the seafloor (100–500 g h
-1
during [500 h over several km
2
) at 300 and 650 m
(BT =12"C) (Fig. 2B). In the Mediterranean Sea,
benthic deposits of P. atlanticum seem to be a common
feature that are generally unnoticed.
Thaliaceans other than P. atlanticum have also been
recorded at the seabed. Cacchione et al. (1978)
described sinking living/moribound Salpa aspera
Chamisso 1819 in the water column from a series of
ROV observations below 2,500 m (BT =3"C) in the
Hudson Canyon, northwest Atlantic, over 30 days
during summer. Salp bodies were observed rolling
down the canyon. In the same area, Wiebe et al. (1979)
observed a jelly-fall of S. aspera at [2,000 m
(BT =3"C). The carcasses accumulated in channels
and furrows and formed string-like aggregations at the
seabed (see Grassle & Morse-Porteus, 1987; Grassle &
Grassle, 1994). In the Pacific Ocean, Duggins (1981)
reported thousands of Salpa fusiformis Cuvier 1804 in
the intertidal/subtidal environment (BT =4"C) of the
Alaska Gulf over several months. Echinoderms fed
preferentially on the gelatinous resource as soon as it
was available. Recently, in the Red Sea, salps have
formed jelly-falls during spring and after upwelling
(20 m, BT =23"C) although these observations were
not quantified (A. Alamaru pers. comm). In the Sea of
Japan, a doliolid jelly-fall was studied in the water
column by means of a sediment trap below 150 m
(temperature =12"C) (Takahashi et al., 2010).
Cnidarians
For Cnidaria, the first natural jelly-fall recorded was in
a photographic survey (Jumars, 1976) below 1,000 m
(BT =4"C), where ophiuroids congregated around a
Pelagia sp. carcass in the Santa Catalina basin
(northeast Pacific). More recently, jelly-falls of Aur-
elia limbata Brandt 1835, Parumbrosa polylobata
Kishinouye 1910, and Nemopilema nomurai Kish-
inouye 1922 were reported on the seafloor down to
400-m depth (BT =2.2–10"C) in the Sea of Japan
during summer and autumn (Miyake et al., 2002,
2005; Yamamoto et al., 2008, respectively). Thou-
sands of Crambionella orsini Vanho
¨ffen 1888 car-
casses were photographed using a towed camera at the
seabed during winter and after seasonal upwelling in
the Arabian Sea (Billett et al., 2006). Carcasses were
recorded as freshly deposited on the shelf, while ‘jelly-
lakes’ of decomposing detritus were observed on the
continental rise deeper than 3,000 m (BT =2"C).
White mats, assumed to be bacteria decomposing and
remineralizing the organic material, covered the
detritus. A scyphozoan jelly-fall (probably C. orsini)
also was reported near the Pakistan Margin at 900 m
(BT =9.5"C) during summer and after seasonal
upwelling (Murty et al., 2009). A large gelatinous
mat covering the seabed, presumably scyphozoans in a
very advanced state of decomposition, was surveyed
for 7 days with a ROV in the Norwegian Sea at
1,380 m (BT =-1"C) during summer (Jones et al.,
2010). A jelly-fall of Periphylla periphylla (Peron &
Lesueur, 1810) was studied in spring 2011 in the
Lurefjorden, Norway between 396 and 443 m
(BT =7"C) (Sweetman & Chapman, 2011). Car-
casses were documented with a camera in two
Hydrobiologia
123

different areas in seven transects at very low densities
(0.01 carcass m
-2
), estimated to contribute \1% to
the annual organic matter flux in the area. Numerous
jelly-falls of Aurelia aurita Linnaeus 1758 occurred
during spring and after upwelling events at 20-m depth
in the Red Sea (BT =23"C) (Alamaru et al., 2009).
Sexton et al. (2010) reported a jelly-fall of Chrysaora
quinquecirrha Desor 1848 medusae in a shallow sub-
estuary of Chesapeake Bay during autumn.
Jelly-falls conceptualization
Processes from the euphotic zone to the seabed
A jelly-fall (Fig. 1) starts when gelatinous organisms
die and sink from the so-called death depth subject to
the organisms’ vertical migration and displacement.
Because gelatinous detritus is denser than the sur-
rounding seawater, the corpses sink through the water
Fig. 2 A Global distribution of reported jelly-falls. Also
included are the species that were recorded in each individual
event (see Table 1for detailed information). BObservations of
P. atlanticum jelly-falls at the seabed in the Mediterranean Sea
(from the MEDITS-ES project) (Bertrand et al., 2002).
Numerous jelly-falls occur along the whole western Iberian
Margin. The legend shows the average number of carcasses
observed at each station from 1994 to 2005. Also included are
observations of P. atlanticum in the Tyrrhenian Sea (northwest
Mediterranean Sea) (Sartor et al., 2003). The bathymetric line
(200 m) are from the general bathymetric chart of the oceans
(GEBCO) Digital Atlas (IOC et al., 2003). The dotted line
indicates the zones trawled in the MEDITS project that can be
used to study jelly-falls from trawling data, as proposed in
‘‘Operational oceanography and exploration techniques’’
section
Hydrobiologia
123

column at a rate determined by the material’s size and
excess density (Stokes’ Law) (e.g. Yamamoto et al.,
2008). The organisms can settle at the seabed while
still alive (Wiebe et al., 1979; Gili et al., 2006) and
then die, thus remineralization can start on the seabed.
As it sinks, the material can be consumed by
scavengers and return to the faunal food web or be
remineralized by bacteria (bacterioplankton) and enter
the microbial loop (e.g. Hansson & Norrman, 1995).
Dissolved organic matter (DOM) leaching from living
or dead organisms provides a link to the ‘‘jelly-pump’’
concept (J-DOM) of microbial communities being
fuelled by DOM excretion (Condon & Steinberg,
2008; Niggl et al., 2010; Condon et al., 2011) (Fig. 1).
Microzooplankton and small zooplankton may also
consume J-DOM (e.g. Iguchi et al., 2006; Titelman
et al., 2006; West et al., 2009a). Laboratory incuba-
tions of scyphozoan material using deep (334 m) and
shallow water (\10 m) differed in the remineraliza-
tion time (Iguchi et al., 2006), which was attributed to
the microbial community as well as temperature in
situ. Differences in the lability of gelatinous tissues
(C:N ratios; Larson, 1986), the various rates at which
the different materials sink (Apstein, 1910; Mills,
1981), and rates of scavenging and bacterial mineral-
ization (which may vary with temperature and depth)
greatly influence the extent to which the jelly-fall is
recycled within the water column versus at the seabed
(Fig. 1). Jelly-falls that reach the seafloor may be
transported elsewhere (e.g. along geomorphological
features) (Billett et al., 2006), or retained in situ and
consumed by the local faunal and microbial commu-
nity (Lebrato & Jones, 2009). Leaching of dissolved
compounds fuels production in higher trophic levels
(West et al., 2009a) and biogeochemical processes
such as oxygen consumption in the water and in the
sediment proceed during the organic enrichment
(West et al., 2009b; Sexton et al., 2010). Associated
total alkalinity changes from excess DOM (Hansson &
Norrman, 1995; Hoppe et al., 2010) and the non-
Redfield stoichiometry of nitrogen and phosphorus
leaching from the corpses (Pitt et al., 2009; Condon
et al., 2010; Tinta et al., 2010) should also be
considered. The decomposition dynamics has been
the focus of several papers targeting a variety of
species at different temperatures, thus decay rates
(k) are available (e.g. Titelman et al., 2006). The
turnover of J-POM is rapid during the first few days
(Sempere et al., 2000) and then slows down, but it is
highly dependent on temperature (Iguchi et al., 2006).
These quantitative data on decomposition dynamics
have enabled remineralization of sinking carcasses to
be modelled in open ocean conditions (Lebrato et al.,
2011). They provided a new metrics based on decay
rate, temperature fields, ‘death depth’, and sinking
speed that helps to understand why different gelati-
nous zooplankton groups transfer organic carbon to
the seabed (e.g. scyphozoans and thaliaceans), while
others may be completely remineralized in the water
column.
The transport to the seafloor of J-POM is an
important source of labile material to the whole size-
spectrum of benthic communities in continental mar-
gins and the deep-sea (Table 1; Fig. 1). Evidence of
organisms consuming J-POM at the seabed has
accumulated slowly from photographs and videos
(Table 1; Fig. 2A). Gelatinous material has a low
energy content (0.5–6 gross energy kJ g dry mass
-1
)
compared to other types of carrion such as fish (5–22
gross energy kJ g dry mass
-1
) or algae ([10 gross
energy kJ g dry mass
-1
) (Doyle et al., 2007). Among
gelatinous species, the energy content is highest in
salps and pyrosomids (4–6 gross energy kJ g dry
mass
-1
) (Davenport & Balazs, 1991; Clarke et al.,
1992), which are important parts of the diets of
numerous benthic organisms (Table 3). Although high
energy resources are readily available on continental
margins, food is a limiting factor in the deep-sea (Gage
& Tyler, 1991). Thus, jelly-falls may represent a
valuable nutritional input at certain times of the year
(Table 3). Unlike other large food falls, which are
usually sparsely scattered over the sea floor, gelatinous
corpses accumulate in large patches (Billett et al.,
2006; Lebrato & Jones, 2009) making it easier for
scavengers to locate; however, scavengers tradition-
ally observed around fish falls (such as isopods or fish)
have not been observed around jelly-falls (Sweetman
& Chapman, 2011). The reduced energy spent
searching for food, and the lability of the gelatinous
carrion relative to other sources of detritus, may
compensate for the reduced energy density of the jelly-
falls at least for some scavenger species (Doyle et al.,
2007). Additionally, jelly-falls may provide an envi-
ronment for macrofauna/microbial communities to
proliferate, which, in turn, may be preyed upon by
other taxa (Sweetman & Chapman, 2011). Sessile
organisms (anthozoans, including hexacorallians, oc-
tocorallians, and scleractians) also consume J-POM
Hydrobiologia
123

(Gili et al., 2006; Alamaru et al., 2009; Lebrato &
Jones, 2009). Echinoderms dominate scavenging
observations at any depth, followed by crustaceans
and fish (Table 3). Remains of J-POM (e.g. Cymbulia
peroni De Blainville 1810) are commonly found in
guts of numerous benthic decapods, such as the
Norway lobster Nephrops norvegicus Linnaeus 1758,
the crab Geryon longipes Milne-Edwards 1882
(in Cartes, 1993a), and the squat lobster Munida
tenuimana Sars 1872 (in Cartes, 1993b). J-POM (Iasis
zonaria Pallas 1774, P. atlanticum,P. periphylla) is
also found in the guts of deep shrimps, such as
Plesionika martia Milne-Edwards 1883 (in Fanelli &
Cartes, 2008) or fish (Carrasson & Cartes, 2002;
Drazen et al., 2008; Goldman & Sedberry, 2010). Any
remaining material that is not channelled through
macro/megafaunal scavenging will eventually be
respired by microbial communities (Fig. 1). The
build-up of impermeable gelatinous material (as in
Billett et al., 2006) on the seafloor leads to reductions
in O
2
flux into sediments (West et al., 2009b). This
would favour microbial over metazoan biomass and
remineralization processes, although low seawater O
2
combined with no light slows microbial decomposi-
tion of settling organic matter (Gooday et al., 2010),
and toxic remineralization products (e.g. ammonium
Table 3 Occurrences of jelly-falls and the megafaunal taxa feeding on them
Year Depth (m) Taxon Timing
a
Duration Units Feeding taxa Reference
2011 396–443 P. periphylla Mar—Sp. 1 days Crustaceans
b
Sweetman & Chapman (2011)
2010 150 Doliolids May—Sp. 5 – None Takahashi et al. (2010)
2009 20 Salps Post-upwelling – – Anthozoans Alamaru et al. (unpublished)
2009 20 A. aurita Post-upwelling – – Anthozoans Alamaru et al. (2009)
2009 900 C. orsini Post-upwelling – – None Murty et al. (2009)
2009 1,380 Scyphozoans Jun—S 7 days None Jones et al. (2010)
2007 3 C. xamachana Sep—S – – None M. Lebrato (unpublished)
2006 146–354 N. nomurai Sep/Oct—S/A 30 days Crustaceans,
echinoderms
Yamamoto et al. (2008)
2006 26–1,275 P. atlanticum Post-upwelling 60 days Several
c
Lebrato & Jones (2009)
2005 1.5–3 C. quinquecirrha Jun/Sep—S 90 days None Sexton et al. (2010)
2003 304–3,299 C. orsini Post-upwelling 17 – Crustaceans,
echinoderms
Billett et al. (2006)
2002 453 P. polylobata Sep—S – – Echinoderms Miyake et al. (2005)
2001 320 A. limbata Aug—S – – Echinoderms Miyake et al. (2002)
1999 300–650 P. atlanticum Sp./S 3 months None Sartor et al. (2003)
1998 300–650 P. atlanticum Sp./S 3 months None Sartor et al. (2003)
1997 300–650 P. atlanticum Sp./S 3 months None Sartor et al. (2003)
1996 300–650 P. atlanticum Sp./S 3 months None Sartor et al. (2003)
1995 300–650 P. atlanticum Sp./Sum 3 months None Sartor et al. (2003)
1985 5,433 P. atlanticum Jun/Jul—S 17 days Crustaceans,
echinoderms
Roe et al. (1990)
1978 1–10 S. fusiformis Mar/Jun—Sp./S 3 months Echinoderms Duggins (1981)
1975 2,500–3,000 S. aspera Aug—S – – None Cacchione et al. (1978)
1975 2,000–3,000 S. aspera Aug—S 4 days None Wiebe et al. (1979)
1955 330–640 P. atlanticum Jun/Jul—S – – Fish Cowper (1960)
1952 100 P. atlanticum Oct–Sp. – – Fish Hurley & McKnight (1959)
a
The month is abbreviated (when available), and the season is indicated as: Sp. spring, Ssummer, Aautumn, WWinter
b
Caridean shrimps grazed on carcasses, and density was higher around jelly-falls compared to non jelly-falls settings. Galatheid
crabs were observed near carcasses, but no grazing was observed
c
Anthozoans, crustaceans, echinoderms, fish, arthropods, polychaetes
Hydrobiologia
123

and free sulphides) could accumulate and seriously
impact sediment biota as well as pelagic ecosystems
(Titelman et al., 2006; Pitt et al., 2009) (Fig. 1).
Ultimately, jelly-falls could induce spatial heteroge-
neity in the biodiversity of benthic communities
(Gooday et al., 2010) as a consequence of the mass
accumulation of undegraded labile material.
Causes and seasonality of jelly-falls
Factors driving the onset of jelly-falls are mostly
linked to the ageing and end of a bloom (Purcell et al.,
2001) and a long-term cumulative effect of negative
factors, such as parasitism, starvation, infection, and
predation (Mills, 1993), with subsequent deposition at
the seabed if the material is not completely reminer-
alized while sinking. In other cases, the material floats
and it is washed ashore (e.g. Pakhomov et al., 2003;
Houghton et al., 2007). The life history of individual
species dictates their fate, although some generalities
apply to all groups, such as seasonal disappearance
from the waters (Mills, 1993). Life cycles are often
completed within a year or a few months, with
subsequent death (see Franqueville, 1971; Mills,
1993). For thaliaceans, there is evidence that high
concentrations of particles and suspended organic
matter [e.g. chlorophyll a[1 mg m
-3
; Perissinotto &
Pakhomov (1998)] clog their feeding apparatus caus-
ing death (Acun
˜a, 2001) despite food being abundant
(Harbison et al., 1986; Zeldis et al., 1995). This
explains the salp jelly-fall studied by Duggins (1981)
in the subtidal zone in Alaska and the beaching of salps
reported by Pakhomov et al. (2003) in the Southern
Ocean. Thaliacean jelly-falls tend to appear at the
seabed after strong periods of upwelling (Lebrato &
Jones, 2009) or after the spring bloom months when
chlorophyll alevels are high (Wiebe et al., 1979;
Duggins, 1981; Roe et al., 1990) (Table 3).
Re-assessment of the season (n=24) when carcasses
of all groups arrive at the seabed indicates that [75%
of jelly-falls occur after the spring bloom in temperate/
subpolar areas and[25% in post-upwelling periods in
the tropics. This happens irrespectively of the depth at
which they are deposited. It remains unclear for
thaliaceans if the concentration or particles per se
causes clogging and subsequent death, or if the
biological composition of the particles and autotroph
community play a role. Potential connections between
climate and gelatinous zooplankton populations in the
water column and the jelly-falls at the seabed have not
yet been investigated. In tropical areas, monsoon
patterns trigger upwelling events that alter water
column properties (e.g. lower temperature, high
nutrients and chlorophyll a, high DOM levels, higher
POM export) (Coble et al., 1998; Honjo et al., 1999),
thus forcing in these zones is different than in
temperate/subpolar latitudes.
In the Cnidaria, several variables may trigger the
onset of jelly-falls, including sudden or sustained
changes in temperature exceeding physiological per-
formance (Gatz et al., 1973) (relevant in upwelling
systems where organisms can experience rapid
changes in the water mass properties due to physical
forcing), ageing of the bloom followed by food
depletion (causing starvation and poor nutrition)
(Mills, 1993; Purcell et al., 2001; Sexton et al.,
2010). The latter cause may have relevance for the
C. orsini carcasses studied by Billett et al. (2006) and
the depositions of N. nomurai observed by Yamamoto
et al. (2008). The food exhaustion hypothesis would
explain why we often observe scyphozoan jelly-falls
after the spring bloom but predominantly in the late
spring/early summer months (Table 3). Other factors
include grazing damage (Arai, 2005), parasitism/
injury/viral infections (Mills, 1993), senescence
(Sexton et al., 2010), extreme weather events trigger-
ing large changes in physical properties of water
(Cargo, 1976), and sinking driven by low temperatures
and inducing deposition and later death owing to
temperature changes (Sexton et al., 2010).
Operational oceanography and exploration
techniques
The jelly-fall concept originates from a handful of
studies undertaken in the field that either described
accidental encounters or, in few cases, targeted known
gelatinous depositions. In[80% of the cases (n=22),
ROV video and/or towed/still cameras were used as
the sampling technique (Table 1). Unless a large area
was covered and transects used to count individual
carcasses (Billett et al., 2006; Lebrato & Jones, 2009),
these techniques remain qualitative (Roe et al., 1990;
Miyake et al., 2002,2005; Yamamoto et al., 2008).
Other techniques, including scuba diving and sedi-
ment traps account for \5% of the observations.
Hydrobiologia
123

Trawling is the only other technique that allows large
quantitative studies (MEDITS-ES dataset; Sartor
et al., 2003). Field work has been accompanied by a
series of laboratory or mesocosm studies that target
associated biogeochemical processes (e.g. Sempere
et al., 2000; Pitt et al., 2009; Tinta et al., 2010).
Although we now have important information about
the occurrence of jelly-falls and their potential influ-
ence on elemental cycling, we still lack combined
effort and large-scale projects on this topic. Temporal
monitoring can be addressed by ‘ocean observatories’
(Table 2; Claustre et al., 2010; Send et al., 2010).
From these ocean observatory initiatives (e.g. EUR-
OCEANS, OceanSITES, ESONET) and scientific
projects that collaborate with offshore industries
(e.g. SERPENT (Jones, 2009), DELOS (http://www.
delos-project.org/), and HAUSGARTEN (Soltwedel
et al., 2005), regular access to the deep-sea will
increase our chances of making informative observa-
tions. We need to move beyond the present semi-
empirical state of understanding to local or regional
monitoring and quantification of jelly-falls. ROVs,
AUVs (autonomous underwater vehicles), benthic
landers, and towed, drop, and time-lapse cameras
should be used (Table 2). In particular, the use of
repeated AUV surveys or a network of time-lapse
cameras strategically placed at the seabed in areas
where jelly-falls have been observed could provide
insights into seasonality and decomposition at the
seabed. Benthic crawlers (Karpen et al., 2007) can
survey inaccessible areas where jelly-falls have been
observed via a optical cable from a shore-based station
for long periods of time.
For large-scale quantification of jelly-falls, log-
books of bottom-trawling surveys from historical to
present times are a unique tool that have not fully
utilized. They mainly target commercial demersal fish
and crustaceans species, but non-commercial or
‘discarded’ (bycatch) species, including gelatinous
zooplankton, are sometimes consistently recorded
(e.g. Sartor et al., 2003; Sanchez et al., 2003; Bastian
et al., 2011). Data from jelly-falls have been collected
in this way (Fig. 2B) and also data on living biomass
(Bastian et al., 2011). Many benthic trawling pro-
grammes exist worldwide [e.g. MEDITS (Interna-
tional bottom trawl survey in the Mediterranean Sea)
(Bertrand et al., 2002); Relini (2000) (Italian Seas);
Sartor et al. (2003) (Tyrrhenian Sea); International
Bottom Trawl Survey (ITBS); NOAA Gulf of Alaska
bottom trawl survey; NEFSC bottom trawl survey
(Gulf of Maine Area); Wilkins et al. (1998) (The 1995
Pacific West Coast bottom trawl survey); Bastian et al.
(2011) (North Atlantic Ocean)]. Information could
also be retrieved from fisheries information net-
works [e.g. PacFIN (http://pacfin.psmfc.org/index.php);
AKFIN (http://www.akfin.org)]; and from state and
wildlife agencies and fishery management councils
(e.g. http://pacfin.psmfc.org/pacfin_pub/links.php)].
Trawling surveys normally cover specific depth ranges
in the so-called trawlable areas in the shelves and
slopes. The surveys do not normally work beyond the
continental slope [(e.g. 0–800 m in the MEDITS-ES,
250–800 m in Sartor et al. (2003)] (Fig. 2B), but
effectively sample the shelves consistently and
repeatedly. The problem often is that to reduce cost
and effort and increase efficiency, the size, weights,
and numbers only of commercial species are recorded
in logbooks, and the living and dead gelatinous com-
ponent, if present, is overlooked. This issue was dis-
covered in the MEDITS-ES project, where certain
partners recorded the same data for commercial and
for non-commercial species (jelly-fall data used in
Fig. 2B), while the majority did not. Only through
effective science-industry communication and col-
laboration can we make use of their potential to
quantify jelly-falls and living biomass (Bastian et al.,
2011).
At local scales, we suggest use of acoustic/
electronic tagging (e.g. Seymour et al., 2004; Gordon
& Seymour, 2008; Hays et al., 2008) on individuals
found in blooms to discover their fate (Table 2). Tags
can be mechanically secured in cnidarians in the bell
area and peduncle, or using setting glue. Large
neutrally buoyant sediment traps also could be used
(Lampitt et al., 2008) that could drift under blooms, as
well as free-drifting profilers with mounted cameras to
investigate the water column. Genetic tools (e.g.
Reusch et al., 2010) could also be used to characterize
a jelly-fall signature in the sediment. Further research
should quantify and study the diversity of the
scavenging communities attracted to an ‘artificial’
jelly-fall (e.g. Yamamoto et al., 2008). This has
traditionally been done with a bait in the field of view
of a still camera (reviewed by Bailey et al., 2007). This
can be combined with labelling studies to assess the
fate of jelly-derived organic material, as for phytode-
tritus (Middelburg et al., 2000; Witte et al., 2003;
Franco et al., 2008).
Hydrobiologia
123

Can jelly-falls provide ecosystem services
in the future?
The future ocean is expected to be a warmer, more-
stratified, acidic, and oxygen-poor system character-
ized by reduced upwelling (Cox et al., 2000; Gregg
et al., 2003). As a result, production exported to depth
is expected to be reduced as phytoplankton commu-
nities shift from large diatom-based assemblages to
picoplankton with lower export efficiency (Buesseler
et al., 2007; Smith et al., 2008). Reduced export
production and changes in community structure are
expected to result in reduced delivery to, and an
overall change in the composition of organic material
reaching the abyssal ocean floor (Laws, 2004; Smith
et al., 2008). This is expected to reduce food
availability to the already food-limited deep-sea floor,
causing a decline in deep-sea biomass and ecosystem
changes (e.g. in faunal behaviour (Kaufmann & Smith,
1997; Wigham et al., 2003), bioturbation (Smith et al.,
2008; Vardaro et al., 2009), faunal densities (Ruhl &
Smith, 2004; Ruhl, 2007,2008; Smith et al., 2008),
reproductive traits (Tyler, 1988; Young, 2003;
Ramirez-Llodra et al., 2005), faunal diversity (Levin
et al., 2001), body size (McClain et al., 2005),
taxonomic composition (Ruhl & Smith, 2004), sedi-
ment infaunal response (Sweetman & Witte, 2008a,
b), and dominance (Cosson et al., 1997; Sweetman &
Witte, 2008b). Reduced carbon export may also
inhibit the ocean’s ability to sequester carbon (Smith
et al., 2008). The potential consequences of the
combination of altered food inputs to the benthos
and increased CO
2
content of seawater on ecosystem
functioning and services (e.g. nutrient regeneration,
energy transfer to higher trophic levels) could have
large implications because recent studies suggest that
an organism’s ability to cope with acidification and
elevated water temperatures may be regulated by food
supply (Wood et al., 2008; Gooding et al., 2009).
Gelatinous zooplankton populations, on the other
hand, may benefit from anthropogenic impacts on the
marine environment (Purcell et al., 2007; Purcell,
2012). There is evidence of some populations increas-
ing during the last decades, such as thaliaceans in the
Southern Ocean (Loeb et al., 1997; Atkinson et al.,
2004) and jellyfish in the Mediterranean Sea
(Molinero et al., 2008). It has been suggested that
jelly-biomass will become an increasingly important
component in the future ocean (Purcell et al., 2007;
Jackson, 2008; Richardson et al., 2009; Purcell, 2012).
Therefore, if classic POM vectors (e.g. phytodetritus)
become less important in the future ocean, an
increased amount of J-POM sinking to the seabed
could mitigate some of the losses of carbon from
phytoplanktonic carbon sources, although it is likely to
be much more heterogeneous at the seafloor
(Gooday et al., 2010). Because the majority of jelly-
falls deposits are located in deep, cold (\10"C)
marine environments (Table 1), we hypothesize that
J-POM:phytodetrital-POM flux ratios are likely to be
higher in deep-sea and polar settings (Lebrato et al.,
2011). This may maintain certain ecosystem functions
in some areas (dependent on the threshold POM flux)
by ensuring a continued minimum POM flux from the
surface to the seafloor. It is also likely to have drastic
implications for benthic community composition just
as changes in surface phytoplankton community
composition can substantially modify abyssal com-
munity composition.
Acknowledgments We are grateful to the scientific and environ-
mental ROV partnership using existing industrial technology
project (SERPENT) for enabling access to data off west Africa
and in the deep Norwegian Sea. We thank the following contri-
butions from individuals: L. Gil de Sola, C. Garcı
´a, J. Pe
´rez Gil, and
P. Abello
´from the I.E.O (Fuengirola Oceanographic Center, Spai n)
for the facilities providing MEDITS-ES data, Brian J. Bett and
R. S. Lampitt from the National Oceanography Center
Southampton, UK provided unpublished data of C. orsini from
Billett et al. (2006)andfromRoeetal.(1990). This work was also
supported by the ‘‘European Project on Ocean Acidification’’
(EPOCA), which is funded from the European Community’s
Seventh Framework Programme (FP7/2007–2013) under grant
agreement no 211384. EPOCA is endorsed by the International
Programmes IMBER, LOICZ and SOLAS. This work was funded
by the grant Becas mineras. exp. 210001 to M. Lebrato and by the
Kiel Cluster of Excellence ‘‘The Future Ocean’’ (D1067/87).
References
Acun
˜a, J. L., 2001. Pelagic tunicates: why gelatinous? The
American Naturalist 158: 100–107.
Alamaru, A., O. Bronstein, G. Dishon & Y. Loya, 2009.
Opportunistic feeding by the fungid coral Fungia scruposa
on the moon jellyfish Aurelia aurita. Coral Reefs 28: 865.
Alldredge, A. L. & M. W. Silver, 1988. Characteristics,
dynamics and significance of marine snow. Progress in
Oceanography 20: 41–82.
Apstein, C., 1910. Hat ein Organismus in der Tiefe Gelebt, in
der er gefischt ist? Internationale Revue der gesamten
Hydrobiologie und Hydrographie 3: 17–33.
Arai, M. N., 2005. Predation on pelagic coelenterates: a review.
Journal of the Marine Biological Association of the United
Kingdom 85: 523–536.
Hydrobiologia
123

Atkinson, A., V. Siegel, E. Pakhomov & P. Rothery, 2004.
Long-term decline in krill stock and increase in salps
within the Southern Ocean. Nature 432: 100–103.
Bailey, D. M., N. J. King & I. G. Priede, 2007. Cameras and
carcasses: historical and current methods for using artificial
food falls to study deep-water animals. Marine Ecology
Progress Series 350: 179–191.
Balch, W., D. Drapeau, B. Bowler & E. Booth, 2007. Prediction
of pelagic calcification rates using satellite measurements.
Deep Sea Research II 54: 478–495.
Bastian, T., D. Stokes, J. E. Kelleher, G. C. Hays, J. Davenport
& T. K. Doyle, 2011. Fisheries bycatch data provide
insights into the distribution of the mauve stinger (Pelagia
noctiluca) around Ireland. ICES Journal of Marine Science
68: 436–443.
Beaulieu, S. E., 2002. Accumulation and fate of phytodetritus on
the sea floor. Oceanography and Marine Biology Annual
Review 40: 171–232.
Behrenfeld, M. J. & P. G. Falkowski, 1997. Photosynthetic rates
derived from satellite-based chlorophyll concentration.
Limnology and Oceanography 42: 1–20.
Bertrand, J. A., L. Gil de Sola, C. Papaconstantinou, G. Relini &
A. Souplet, 2002. The general specifications of the Medits
surveys. In Abello, P., J. A. Bertrand, L. Gil de Sola, C.
Papaconstantinou, G. Relini & A. Souplet (eds), Mediter-
ranean Marine Demersal Resources, The MEDITS Inter-
national Trawl Survey (1994–1999). Scientia Marina 66:
9–17.
Billett, D. S. M., B. J. Bett, C. L. Jacobs, I. P. Rouse & B.
D. Wigham, 2006. Mass deposition of jellyfish in the deep
Arabian Sea. Limnology and Oceanography 51: 2077–2083.
Buesseler, K. O., M. P. Bacon, K. Cochran & H. D. Livingston,
1992. Carbon and nitrogen export during the JGOFS North
Atlantic Bloom Experiment estimated from
234
Th,
238
U
disequilibria. Deep Sea Research I 39: 1115–1137.
Buesseler, K. O., C. H. Lamborg, P. W. Boyd, P. J. Lam, T.
W. Trull, R. R. Bidigare, J. K. B. Bishop, K. L. Casciotti, F.
Dehairs, M. Elskens, M. Honda, D. M. Karl, D. A. Siegel,
M. A. Silver, D. K. Steinberg, J. Valdes, B. Van Mooy & S.
Wilson, 2007. Revisiting carbon flux through the ocean’s
twilight zone. Science 316: 567–570.
Burd, A. B., D. A. Hansell, D. K. Steinberg, T. R. Anderson, J.
Aristegui, F. Baltar, S. R. Beaupre, K. O. Buesseler, F.
DeHairs, G. A. Jackson, D. C. Kadko, R. Koppelmann, R.
S. Lampitt, T. Nagata, T. Reinthaler, C. Robinson, B.
H. Robison, C. Tamburini & T. Tanaka, 2010. Assessing
the apparent imbalance between geochemical and bio-
chemical indicators of meso- and bathypelagic biological
activity, What the @$#! is wrong with present calculations
and carbon budgets? Deep Sea Research II 57: 1557–1571.
Cacchione, D. A., G. T. Rowe & A. Malahoff, 1978. Sub-
mersible investigation of outer Hudson submarine canyon.
In Stanley, D. J. & G. Kelling (eds), Sedimentation in
Canyons, Fans and Trenches. Dowden, Hutchinson and
Ross, Stroudsburg: 42–50.
Cargo, D. G., 1976. Some effects of tropical storm Agnes on the
sea nettle population in the Chesapeake Bay. In Davis, J. &
B. Laird (eds), The Effects of Tropical Storm Agnes on the
Chesapeake Bay Estuarine System. Chesapeake Bay
Consortium 54. Johns Hopkins University Press, Balti-
more: 417–424.
Caron, D. A., P. G. Davis, L. P. Madin & J. M. Sieburth, 1986.
Enrichment of microbial populations in macroaggregates
(marine snow) from surface waters of the North Atlantic.
Journal of Marine Research 44: 543–565.
Carrasson, M. & J. E. Cartes, 2002. Trophic relationships in a
Mediterranean deep-sea fish community partition of food
resources, dietary overlap and connections within the
benthic boundary layer. Marine Ecology Progress Series
241: 41–55.
Cartes, J. E., 1993a. Diets of deep-water pandalid shrimps on the
Western Mediterranean slope. Marine Ecology Progress
Series 96: 49–61.
Cartes, J. E., 1993b. Diets of two deep-sea decapods Nemato-
carcinus exilis (Caridea: Nematocarcinidac) and Munida
tenuimana (Anomura: Galatheidae) on the Western Med-
iterranean slope. Ophelia 37: 213–229.
Cartes, J. E., V. Papiol, A. Palanques, J. Guillen & M. Demestre,
2007. Dynamics of suprabenthos off the Ebro Delta (Cat-
alan Sea, western Mediterranean), spatial and temporal
patterns and relationships with environmental factors.
Estuarine, Coastal and Shelf Science 75: 501–515.
Cartes, J. E., F. Maynou, E. Fanelli, C. Romano, V. Mamouridis
& V. Papiol, 2009. The distribution of megabenthic,
invertebrate epifauna in the Balearic Basin (Western
Mediterranean) between 400 and 2300 m: environmental
gradients influencing assemblages composition and bio-
mass trends. Journal of Sea Research 66: 244–257.
Cartes, J. E., E. Fanelli, V. Papiol & F. Maynou, 2010. Trophic
relationships at interannual spatial and temporal scales of
macro and megafauna around a submarine canyon off the
Catalonian coast (western Mediterranean). Journal of Sea
Research 63: 180–190.
Clarke, A., L. J. Holmes & D. J. Gore, 1992. Proximate and
composition of gelatinous zooplankton from the Southern
Ocean. Journal of Experimental Marine Biology and
Ecology 155: 55–68.
Claustre, H., J. Bishop, E. Boss, S. Bernard, J-F. Berthon, C.
Coatanoan, K. Johnson, A. Lotiker, O. Ulloa, M. J. Perry,
F. D’Ortenzio, O. H. F. D’andon & J. Uitz, 2010. Bio-
optical profiling floats as new observational tools for bio-
geochemical and ecosystem studies: potential synergies
with ocean colour remote sensing. OceanObs’09, Venice,
September 21–25.
Coble, P. G., C. E. del Castillo & B. Avril, 1998. Distribution
and optical properties of CDOM in the Arabian Sea during
the 1995 Southwest Monsoon. Deep Sea Research II 45:
2195–2223.
Condon, R. H. & D. K. Steinberg, 2008. Development, bio-
logical regulation, and fate of ctenophore blooms in the
York River estuary, Chesapeake Bay. Marine Ecology
Progress Series 369: 153–168.
Condon, R. H., D. K. Steinberg & D. A. Bronk, 2010. Production
of dissolved organic matter and inorganic nutrients by
gelatinous zooplankton in the York River estuary, Chesa-
peake Bay. Journal of Plankton Research 32: 153–170.
Condon, R. H., D. K. Steinberg, P. A. del Giorgio, T. C. Bouvier,
D. A. Bronk, W. A. Graham & H. W. Ducklow, 2011.
Jellyfish blooms result in a major microbial respiratory sink
of carbon in marine systems. Proceedings of the National
Academy of Sciences of the United States of America 108:
10225–10230.
Hydrobiologia
123

Conte, M. H., T. D. Dickey, J. C. Weber, R. J. Johnson & A.
H. Knap, 2003. Transient physical forcing of pulsed export
of bioreactive material to the deep Sargasso Sea. Deep Sea
Research I 50: 1157–1187.
Cosson, N., M. Sibuet & J. Galeron, 1997. Community structure
and spatial heterogeneity of the deep-sea macrofauna at
three contrasting stations in the tropical northeast Atlantic.
Deep Sea Research I 44: 247–269.
Cowper, T. R., 1960. Occurrence of Pyrosoma on the conti-
nental Slope. Nature 187: 878–879.
Cox, P. M., R. A. Bets, C. D. Jones, S. A. Spall & I. J. Totterdell,
2000. Acceleration of global warming due to carbon-cycle
feedbacks in a coupled climate model. Nature 408: 184–187.
Davenport, J. & G. H. Balazs, 1991. ‘‘Fiery pyrosomas’’: are
pyrosomas an important items in the diet of leatherback
turtles? British Herpetological Society Bulletin 37: 33–38.
Doyle, T. K., D. R. Houghton, R. McDevitt, J. Davenport & G.
C. Hays, 2007. The energy density of jellyfish: estimates
from bomb-calorimetry and proximate-composition.
Journal of Experimental Marine Biology and Ecology 343:
239–252.
Drazen, J. C., B. N. Popp, C. A. Choy, T. Clemente, L. de Forest
& K. L. Smith, 2008. Bypassing the abyssal benthic food
web: macrourid diet in the eastern North Pacific inferred
from stomach content and stable isotopes analyses. Lim-
nology and Oceanography 53: 2644–2654.
Duggins, D. O., 1981. Sea urchins and kelp, the effects of short
term changes in urchin diet. Limnology and Oceanography
26: 391–394.
Fanelli, E. & J. E. Cartes, 2008. Spatio-temporal variability in
the diet of two pandalid shrimps in the western Mediter-
ranean evidenced from gut contents and stable isotope
analysis: in-fluence on the reproductive cycle. Marine
Ecology Progress Series 355: 219–233.
Franco, M. A., K. Soetaert, M. J. Costa, M. Vincx & J. Vana-
verbeke, 2008. Uptake of phytodetritus by meiobenthos
using
13
C labelled diatoms and Phaeocystis in two con-
trasting sediments from the North Sea. Journal of Experi-
mental Marine Biology and Ecology 362: 1–8.
Franqueville, C., 1971. Macroplancton profond (inverte
´bre
´s) de
la Me
´diterrane
´e nord-occidentale. Tethys 3: 11–56.
Gage, J. D. & P. A. Tyler, 1991. Deep-Sea Biology: A Natural
History of Organisms at the Deep-sea Floor. Cambridge
University Press, Cambridge.
Gatz, A. J., V. S. Kennedy & J. A. Mihursky, 1973. Effects of
temperature on activity and mortality of the scyphozoan
medusa Chrysaora quinquecirrha. Chesapeake Science 14:
171–180.
Gili, J.-M., S. Rossi, F. Pages, C. Orejas, N. Teixido, P. J. Lopez-
Gonzalez & W. E. Arntz, 2006. A new trophic link between
the pelagic and benthic systems on the Antarctic shelf.
Marine Ecology Progress Series 322: 43–49.
Goldman, S. F. & G. R. Sedberry, 2010. Feeding habits of some
demersal fish on the Charleston Bump off the southeastern
United States. ICES Journal of Marine Science 68:
390–398.
Gooday, A. J., B. J. Bett, E. Escobar, B. Ingole, L. A. Levin, C.
Neira, A. V. Raman & J. Sellanes, 2010. Habitat hetero-
geneity and its influence on benthic biodiversity in oxygen
minimum zones. Marine Ecology 31: 125–147.
Gooding, R., C. Harley & E. Tang, 2009. Elevated water tem-
perature and carbon dioxide concentration increase the
growth of a keystone echinoderm. Proceedings of the
National Academy of Sciences of the United States of
America 106: 9316–9321.
Gordon, M. R. & J. E. Seymour, 2008. Quantifying movement
of the tropical Australian cubozoan Chironex fleckeri using
acoustic telemetry. Hydrobiologia 616: 87–97.
Grassle, J. F. & J. P. Grassle, 1994. Notes from the abyss, the
effects of a patchy supply of organic material and larvae on
soft-sediment benthic communities. In Giller, P. S., A.
G. Hildrew & D. G. Raffaelli (eds), Aquatic Ecology, Scale,
Pattern and Process, 34th Symposium of the British Eco-
logical Society. Blackwell Scientific, Oxford: 499–515.
Grassle, J. F. & L. S. Morse-Porteus, 1987. Macrofaunal colo-
nization of disturbed deep-sea environments and the
structure of deep-sea benthic communities. Deep Sea
Research I 34: 1911–1950.
Gregg, W., P. Ginoux, P. Schopf & N. Casey, 2003. Phyto-
plankton and iron, validation of a global three-dimensional
ocean biogeochemical model. Deep Sea Research II 50:
3143–3169.
Griffin, D. J. G. & J. C. Yaldwyn, 1970. Giant colonies of
pelagic tunicate (Pyrosoma spinosum) from SE Australia
and New Zealand. Nature 226: 464.
Hansson, L. J. & B. Norrman, 1995. Release of dissolved
organic carbon (DOC) by the scyphozoan jellyfish Aurelia
aurita and its potential influence on the production of
planktic bacteria. Marine Biology 121: 527–532.
Harbison, G. R., V. L. McAlister & R. W. Gilmer, 1986. The
response of the salp, Pegea confoederata, to high levels of
particulate material: starvation in the midst of plenty.
Limnology and Oceanography 31: 371–382.
Hays, G. C., T. K. Doyle, J. D. R. Houghton, M. K. S. Lilley, J.
D. Metcalfe & D. Righton, 2008. Diving behaviour of
jellyfish equipped with electronic tags. Journal of Plankton
Research 30: 325–331.
Honjo, S., J. Dymond, W. Prell & V. Ittekkot, 1999. Monsoon-
controlled export fluxes to the interior of the Arabian Sea.
Deep Sea Research II 46: 1859–1902.
Hoppe, C. J. M., G. Langer, S. D. Rokitta, D. A. Wolf-Gladrow
& B. Rost, 2010. On CO
2
perturbation experiments: over-
determination of carbonate chemistry reveals inconsisten-
cies. Biogeosciences Discussions 7: 1707–1726.
Houghton, J. D. R., T. K. Doyle, J. Davenport, M. K. S. Lilley,
R. P. Wilson & G. C. Hays, 2007. Stranding events provide
indirect insights into the seasonality and persistence of
jellyfish medusae (Cnidaria: Scyphozoa). Hydrobiologia
589: 1–13.
Hurley, D. E. & D. G. McKnight, 1959. Occurrence of Pyro-
soma on the sea-floor 160 metres deep. Nature 183:
554–555.
Iguchi, N., R. Ishikawa, O. Sato, T. Onishi, & T. Maeda, 2006.
Decomposition rate of the giant jellyfish Nemopilema
nomurai in Sado Island. FRA, Japan Sea National Fisheries
Research Institute report. http://jsnfri.fra.affrc.go.jp/Kurage/
kurage_hp18/Sado_bunkai.pdf.
IOC, IHO, and BODC, 2003. Centenary Edition of the GEBCO
Digital Atlas, published on CD-ROM on behalf of the
Intergovernmental Oceanographic Commission and the
Hydrobiologia
123

International Hydrographic Organization as part of the
General Bathymetric Chart of the Oceans. British Ocean-
ographic Data Centre, Liverpool.
Jackson, J. B. C., 2008. Ecological extinction and evolution in the
brave new ocean. Proceedings of the National Academy of
Sciences of the UnitedStates of America 105: 11458–11465.
Jahnke, R. A., 1996. The global ocean flux of particulate organic
carbon, areal distribution and magnitude. Global Biogeo-
chemical Cycles 10: 71–88.
Jiang, S., T. D. Dickey, D. K. Steinberg & L. P. Madin, 2007.
Temporal variability of zooplankton biomass from ADCP
backscatter time series data at the Bermuda Testbed
Mooring site. Deep Sea Research I 54: 608–636.
Johns, B., P. Marsaleix, C. Estournel & R. Vehil, 1992. On the
wind-driven coastal upwelling in the Gulf of Lions. Journal
of Marine Systems 3: 309–320.
Jones, D. O. B., 2009. Using existing industrial remotely oper-
ated vehicles for deep-sea science. Zoologica Scripta 38:
41–47.
Jones, D. O. B., C. N. Roterman & A. R. Gates, 2010. Shell Gro
SERPENT final report. National Oceanography Centre
Southampton, Southampton. National Oceanography Centre
Southampton Research and Consultancy Report: 79.
Jumars, P. A., 1976. Deep-sea species diversity. Does it have a
characteristic scale? Journal of Marine Research 34:
217–246.
Karpen, V., T. Viergutz & L. Thomsen, 2007. Baltic Observa-
tory for Oceanographic Monitoring. Sea Technology, July
2007, 18–20.
Kaufmann, R. S. & K. L. Smith, 1997. Activity patterns of
mobile epibenthic megafauna at an abyssal site in the
eastern North Pacific: results from a 17-month time-lapse
photographic study. Deep Sea Research I 44: 559–579.
Kemp, W. M., E. M. Smith, M. Marvin-DiPasquale & W.
R. Boynton, 1997. Organic carbon balance and net eco-
system metabolism in Chesapeake Bay. Marine Ecology
Progress Series 150: 229–248.
Key, R. M., A. Kozyr, C. L. Sabine, K. Lee, R. Wanninkhof, J.
Bullister, R. A. Feely, F. Millero, C. Mordy & T. H. Peng,
2004. A global ocean carbon climatology, results from
GLODAP. Global Biogeochemical Cycles 18: GB4031.
Lampitt, R. S., B. J. Bett, K. Kiriakoulakis, E. E. Popova, O.
Ragueneau, A. Vangriesheim & G. A. Wolff, 2001.
Material supply to the deep-seafloor in the Northeast
Atlantic. Progress in Oceanography 50: 27–63.
Lampitt, R. S., B. Boorman, L. Brown, M. Lucas, I. Salter, R.
Sanders, K. Saw, S. Seeyave, S. J. Thomalla & R. Turne-
witsch, 2008. Particle export from the euphotic zone:
estimates using a novel drifting sediment trap,
234
Th and
new production. Deep Sea Research I 55: 150–1484.
Larson, R. J., 1986. Water content, organic content, and carbon
and nitrogen composition of medusae from the northeast
Pacific. Journal of Experimental Marine Biology and
Ecology 99: 107–120.
Laws, E. A., 2004. Export flux and stability as regulators of
community composition in pelagic marine biological
communities: implications for regime shifts. Progress in
Oceanography 60: 343–354.
Lebrato, M. & D. O. B. Jones, 2009. Mass deposition event of
Pyrosoma atlanticum carcasses off Ivory Coast (West
Africa). Limnology and Oceanography 54: 1197–1209.
Lebrato, M., M. Pahlow, A. Oschlies, K. A. Pitt, D. O. B. Jones,
J. C. Molinero & R. H. Condon, 2011. Depth attenuation of
organic matter export associated with jelly falls. Limnol-
ogy & Oceanography 56:1917–1928.
Levin, L. A., R. J. Etter, M. A. Rex, A. J. Gooday, C. R. Smith, J.
Pineda, C. T. Stuart, R. R. Hessler & D. Pawson, 2001.
Environmental influences on regional deep-sea species
diversity. Annual Review of Ecology Evolution and Sys-
tematics 32: 51–93.
Loeb, V., V. Siegel, O. Holm-Hansen, R. Hewitt, W. Fraser, W.
Trivelpiece & S. Trivelpiece, 1997. Effects of sea-ice
extent and krill or salp dominance on the Antarctic food
web. Nature 387: 897–900.
Lombard, F. & T. P. Kiorbe, 2010. Marine snow originating
from appendicularian houses: age-dependent settling
characteristics. Deep Sea Research I 57: 1304–1313.
Marchant, M., D. Hebbeln & G. Wefer, 1999. High resolution
planktic foraminiferal record of the last 13:300 years from
the upwelling area off Chile. Marine Geology 61: 115–128.
Martin, J. & J.-C. Miquel, 2010. High downward flux of muci-
laginous aggregates in the Ligurian Sea during summer
2002. Similarities with the mucilage phenomenon in the
Adriatic Sea. Marine Ecology 31: 393–406.
McClain, C. R., M. A. Rex & R. Jabbour, 2005. Deconstructing
bathymetric body size patterns in deep-sea gastropods.
Marine Ecology Progress Series 297: 181–187.
Merckelbach, L. M. & H. Ridderinkhof, 2006. Estimating sus-
pended sediment concentration from ADCP backscatter-
ance at a site with strong tidal currents. Ocean Dynamics
56: 153–168.
Middelburg, J. J., C. Barranguet, H. T. S. Boschker, P. M. J.
Herman, T. Moens & C. H. R. Heip, 2000. The fate of
intertidal microphytobenthos carbon: an in situ
13
C-label-
ing study. Limnology Oceanography 45: 1224–1234.
Mills, C. E., 1981. Diversity of swimming behaviours in
hydromedusae as related to feeding and utilization of
space. Marine Biology 64: 185–189.
Mills, C. E., 1993. Natural mortality in NE Pacific coastal
hydromedusae: grazing predation, wound healing and
senescence. Bulletin of Marine Science 53: 194–203.
Mills, C. E., 2001. Jellyfish blooms: are populations increasing
globally in response to changing ocean conditions? Hyd-
robiologia 451: 55–68.
Miyake, H., D. L. Lindsay, J. C. Hunt & T. Hamatsu, 2002.
Scyphomedusa Aurelia limbata (Brandt, 1838) found in
deep waters off Kushiro, Hokkaido, Northern Japan.
Journal of Plankton Biology and Ecology 49: 44–46.
Miyake, H., D. L. Lindsay, M. Kitamura & S. Nishida, 2005.
Occurrence of the scyphomedusa Parumbrosa polylobata
Kishinouye, 1910 in Suruga Bay, Japan. Journal of
Plankton Biology and Ecology 52: 58–66.
Molinero, J. C., M. Casini & E. Buecher, 2008. The influence of
the Atlantic and regional climate variability on the long-
term changes in gelatinous carnivore populations in the
northwestern Mediterranean. Limnology and Oceanogra-
phy 53: 1456–1467.
Monniot, C. & F. Monniot, 1966. A benthic pyrosoma, Pyro-
soma benthica n. sp. French Academy of Science 263:
368–370.
Moseley, H. N., 1880. Deep-sea dredging and life in te deep sea
III. Nature 21: 591–593.
Hydrobiologia
123

Murty, S. J., B. J. Bett & A. J. Gooday, 2009. Megafaunal
responses to strong oxygen gradients on the Pakistan
margin of the Arabian Sea. Deep Sea Research I 56:
472–487.
Niggl, W., M. S. Naumann, U. Struck, R. Manasrah & C. Wild,
2010. Organic matter release by the benthic upside-down
jellyfish Cassiopea sp. fuels pelagic food webs in coral
reefs. Journal of Experimental Marine Biology and Ecol-
ogy 384: 99–106.
Pakhomov, E. A., V. Fuentes, I. Schloss, A. Atencio & G.
B. Snal, 2003. Beaching of the tunicate Salpa thompsoni at
high levels of suspended particulate matter in the Southern
Ocean. Polar Biology 26: 427–431.
Perissinotto, R. & E. A. Pakhomov, 1998. Contribution of salps
to carbon flux of marginal ice zone of the Lazarev Sea,
Southern Ocean. Marine Biology 131: 25–32.
Pitt, K. A., D. T. Welsh & R. H. Condon, 2009. Influence of
jellyfish blooms on carbon, nitrogen, and phosphorus
cycling and plankton production. Hydrobiologia 616:
133–149.
Purcell, J. E., 2012. Jellyfish and ctenophore blooms coincide
with human proliferations and environmental perturba-
tions. Annual Review of Marine Science 4: 209–235.
Purcell, J. E., W. M. Graham & H. Dumont, 2001. Jellyfish
Blooms: Ecological and Societal Importance. Develop-
ments in Hydrobiology 155 (Hydrobiologia 451). Kluwer
Academic, Dordrecht: 1–333.
Purcell, J. E., S.-I. Uye & W.-T. Lo, 2007. Anthropogenic
causes if jellyfish blooms and their direct consequences for
humans: a review. Marine Ecology Progress Series 350:
153–174.
Ramirez-Llodra, E., W. D. K. Reid & D. S. M. Billett, 2005.
Long-term changes in reproductive patterns of the holo-
thurian Oneirophanta mutabilis from the Porcupine
Abyssal Plain. Marine Biology 146: 683–693.
Relini, G., 2000. Demersal trawl surveys in Italian seas: a short
review. In Bertrand, J. A. & G. Relini (eds), Demersal
Resources in the Mediterranean. Proceedings of the Sym-
posium held in Pisa, 18–21 March 1998. Actes de Collo-
ques 26, 76–93.
Reusch, T. B. H., S. Bolte, M. Sparwel, A. G. Moss & J.
Javidpour, 2010. Microsatellites reveal origin and genetic
diversity of Eurasian invasions by one of the world’s most
notorious marine invader, Mnemiopsis leidyi (Ctenophora).
Molecular Ecology 19: 2690–2699.
Richardson, A. J., A. Bakun, G. C. Hays & M. J. Gibbons, 2009.
The jellyfish joyride, causes, consequences and manage-
ment responses to a more gelatinous future. Trends in
Ecology & Evolution 24: 312–322.
Robison, B. H., K. R. Reisenbichler & R. E. Sherlock, 2005.
Giant larvacean houses, rapid carbon transport to the deep-
sea floor. Science 308: 1609–1611.
Roe, H. S. J., D. S. M. Billett & R. S. Lampitt, 1990. Benthic/
midwater interactions on the Madeira Abyssal Plain; evi-
dence for biological transport pathways. Progress in
Oceanography 24: 127–140.
Rowe, G. T. & N. Staresinic, 1979. Source of organic matter to
the deep-sea benthos. Ambio Special Report 6: 19–23.
Ruhl, H. A., 2007. Abundance and size distribution dynamics of
abyssal epibenthic megafauna in the northeast Pacific.
Ecology 88: 1250–1262.
Ruhl, H. A., 2008. Community change in the variable resource
habitat of the abyssal northeast Pacific. Ecology 89: 991–1000.
Ruhl, H. A. & K. L. Smith, 2004. Shifts in deep-sea community
structure linked to climate and food supply. Science 305:
513–515.
Ruhl, H. A., J. A. Ellena & K. L. Smith, 2008. Connections
between climate, food limitation, and carbon cycling in
abyssal sediment communities. Proceedings of the
National Academy of Sciences of the United States of
America 105: 17006–17011.
Sanchez, P., M. Demestre & P. Martin, 2003. Characterisation
of the discards generated by bottom trawling in the north-
western Mediterranean. Fisheries Research 67: 71–80.
Sartor, P., M. Sbrana & B. Reale, 2003. Impact of the deep sea
trawl fishery on demersal communities of the northern
Tyrrhenian Sea (Western Mediterranean). Journal of the
Northwest Atlantic Fishery Science 31: 275–284.
Sempere, R., S. C. Yoro, F. van Wambeke & B. Charriere, 2000.
Microbial decomposition of large organic particles in the
northwestern Mediterranean Sea: an experimental approach.
Marine Ecology Progress Series 198: 61–72.
Send, U., R. Weller, D. Wallace, F. Chavez, R. S. Lampitt, T.
Dickey, M. Honda, K. Nittis, R. Lukas, M. McPhaden & R.
A. Feely, 2010. OceanSITES. OceanObs’09, Venice,
September 21–25.
Sexton, M. A., R. R. Hood, J. Sarkodee-adoo & A. M. Liss,
2010. Response of Chrysaora quinquecirrha medusae to
low temperature. Hydrobiologia 645: 125–133.
Seymour, J. E., T. J. Carrette & P. A. Sutherland, 2004. Do box
jellyfish sleep at night? Medical Journal of Australia 181:
706.
Smith, C. R. & A. M. Baco, 2003. Ecology of whale falls at the
deep-sea floor. Oceanography and Marine Biology Annual
Review 41: 311–354.
Smith, C. R., F. C. De Leo, A. F. Bernardino, A. K. Sweetman &
P. Martinez-Arbizu, 2008. Abyssal food limitation, eco-
system structure and climate change. Trends in Ecology &
Evolution 23: 518–528.
Soltwedel, T., K. von Juterzenka, K. Premke & M. Klages, 2003.
What a lucky shot! Photographic evidence for a medium-
sized natural food-fall at the deep seafloor. Oceanologica
Acta 26: 5–6.
Soltwedel, T., E. Bauerfeind, M. Bergmann, N. Budaeva, E.
Hoste, N. Jaeckisch, K. von Juterzenka, J. Matthiessen, V.
Mokievsky, E.-V. Nothig, N.-V. Queric, B. Sablotny, E.
Sauter, M. Schewe, B. Urban-Malinga, J. Wegner, M.
Wlodarska-Kowalczuk & M. Klages, 2005. HAUSGAR-
TEN: multidisciplinary investigations at a deep-sea, long-
term observatory in the Arctic Ocean. Oceanography 18:
46–61.
Sweetman, A. K. & A. Chapman, 2011. First observations of
jelly-falls at the seafloor in a deep-sea fjord. Deep Sea
Research I 58: 1206–1211.
Sweetman, A. K. & U. Witte, 2008a. Response of an abyssal
macrofaunal community to a phytodetrital pulse. Marine
Ecology Progress Series 355: 73–84.
Sweetman, A. K. & U. Witte, 2008b. Macrofaunal response to
phytodetritus in a bathyal Norwegian fjord. Deep Sea
Research I 55: 1503–1514.
Takahashi, K., H. Saito, S. Kakehi & K. Hidaka, 2010. Sapphir-
inid copepods as a predator of doliolids, their contribution to
Hydrobiologia
123

doliolids mortality and sinking flux. EOS Transactions
AGU, 91, 26, Ocean Science Meeting. Abstract BO13A-08.
Tinta, T., A. Malej, M. Kos & V. Turk, 2010. Degradation of the
Adriatic medusa Aurelia sp. by ambient bacteria. Hydro-
biologia 1: 179–191.
Titelman, J., L. Riemann, T. A. Sornes, T. Nilsen, P. Griekspoor
& U. Bamstedt, 2006. Turnover of dead jellyfish, stimu-
lation and retardation of microbial activity. Marine Ecol-
ogy Progress Series 325: 43–58.
Turner, R. D., 1973. Wood-boring bivalves, opportunistic spe-
cies in the deep sea. Science 180: 1377–1379.
Turner, J. T., 2002. Zooplankton faecal pellets, marine snow and
sinking phytoplankton blooms. Aquatic Microbiology and
Ecology 27: 57–102.
Tyler, P. A., 1988. Seasonality in the deep sea. Oceanography
and Marine Biology Annual. Review 18: 125–153.
Vardaro, M. F., H. A. Ruhl & K. L. Smith, 2009. Climate var-
iation, carbon flux, and bioturbation in the abyssal North
Pacific. Limnology and Oceanography 54: 2081–2088.
Vetter, E. W. & P. K. Dayton, 1998. Macrofaunal communities
within and adjacent to a detritus-rich submarine canyon
system. Deep Sea Research II 45: 25–54.
Vetter, E. W. & P. K. Dayton, 1999. Organic enrichment by
macrophyte detritus, and abundance patterns of megafa-
unal populations in submarine canyons. Marine Ecology
Progress Series 186: 137–148.
Wefer, G. & G. Fischer, 1993. Seasonal patterns of vertical
particle flux in equatorial and coastal upwelling areas of the
eastern Atlantic. Deep Sea Research I 40: 1613–1645.
West, E. J., K. A. Pitt, D. T. Welsh, K. Koop & D. Rissik, 2009a.
Top-down and bottom-up influences of jellyfish on primary
productivity and planktonic assemblages. Limnology and
Oceanography 54: 2058–2071.
West, E. J., D. T. Welsh & K. A. Pitt, 2009b. Influence of
decomposing jellyfish on sediment oxygen demand and
nutrient dynamics. Hydrobiologia 616: 151–160.
Wiebe, P. H., L. P. Madin, L. R. Haury, G. R. Harbison & L.
M. Philbin, 1979. Diel vertical migration by Salpa aspera
and its potential for large-scale particulate organic matter
transport to the deep-sea. Marine Biology 53: 249–255.
Wigham, B. D., P. A. Tyler & D. S. M. Billett, 2003. Repro-
ductive biology of the abyssal holothurian Amperima
rosea: an opportunistic response to variable flux of surface
derived organic matter? Journal of the Marine Biology
Association of the United Kingdom 83: 175–188.
Wilkins, M. E., M. Zimmernmann & K. L. Weinberg, 1998. The
1995 Pacific West Coast bottom trawl survey of groundfish
resources: estimates of distribution, abundance, and length
and age composition. NOAA technical Memorandum
NMFS-AFSC-89.
Witte, U., N. Aberte, M. Sand & F. Wenzhofer, 2003. Rapid
response of a deep-sea benthic community to POM
enrichment, an in situ experimental study. Marine Ecology
Progress Series 251: 27–36.
Wood, H. L., J. I. Spicer & S. Widdicombe, 2008. Ocean
acidification may increase calcification rates, but at a cost.
Proceedings of the Royal Society B 275: 1767–1773.
Yamamoto, J., M. Hirose, T. Ohtani, K. Sugimoto, K. Hirase, N.
Shimamoto, T. Shimura, N. Honda, Y. Fujimori & T. Mu-
kai, 2008. Transportation of organic matter to the sea floor
by carrion falls of the giant jellyfish Nemopilema nomurai
in the Sea of Japan. Marine Biology 153: 311–317.
Young, C. M., 2003. Reproduction, development and life-his-
tory traits. In Tyler, P. A. (ed.), Ecosystems of the World.
Elsevier Science, Amsterdam: 381–426.
Zeldis, J., C. S. Davis, M. R. James, S. L. Ballara, W. E. Booth &
F. H. Chang, 1995. Salp grazing: effects on phytoplankton
abundance, vertical distribution and taxonomic composi-
tion in a coastal habitat. Marine Ecology Progress Series
126: 267–283.
Hydrobiologia
123