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Research
Cite this article: Hoving HJT, Bush SL,
Haddock SHD, Robison BH. 2017 Bathyal
feasting: post-spawning squid as a source of
carbon for deep-sea benthic communities.
Proc. R. Soc. B 284: 20172096.
http://dx.doi.org/10.1098/rspb.2017.2096
Received: 25 September 2017
Accepted: 20 November 2017
Subject Category:
Ecology
Subject Areas:
ecology
Keywords:
biological carbon pump, deep sea,
Cephalopoda, food falls, nekton
Author for correspondence:
H. J. T. Hoving
e-mail: hhoving@geomar.de
Electronic supplementary material is available
online at https://dx.doi.org/10.6084/m9.
figshare.c.3946252.
Bathyal feasting: post-spawning squid
as a source of carbon for deep-sea
benthic communities
H. J. T. Hoving1, S. L. Bush2,3, S. H. D. Haddock2and B. H. Robison2
1
GEOMAR, Helmholtz Centre for Ocean Research Kiel, Du¨sternbrooker Weg 20, 24105 Kiel, Germany
2
Monterey Bay Aquarium Research Institute, Moss Landing, CA 95039, USA
3
Monterey Bay Aquarium, 886 Cannery Row, Monterey, CA 93940, USA
HJTH, 0000-0002-4330-6507; SLB, 0000-0001-5169-7686
In many oceanic carbon budgets there is a discrepancy between the energetic
requirements of deep-sea benthic communities and the supply of organic
matter. This suggeststhat there are unidentified and unmeasured food sources
reaching the seafloor. During 11 deep-sea remotely operated vehicle (ROV) sur-
veys in the Gulf of California, the remains (squidcarcasses and hatched-out egg
sheets) of 64 post-brooding squid were encountered. As many as 36 remains
were encountered during a single dive. To our knowledge this is one of the lar-
gest numbers of natural food falls of medium-size deep-sea nekton described to
date. Various deep-sea scavengers (Ophiuroidea, Holothuroidea, Decapoda,
Asteroidea, Enteropneusta) were associated with the remains. Although
many of the 80 examined ROV dives did not encounter dead squids or egg
sheets (n¼69), and the phenomenon may be geographically and temporally
restricted, our results show that dead, sinking squid transport carbon from
the water column to the seafloor in the Gulf of California. Based on food fall
observations from individual dives, we estimate that annual squid carcass
depositions may regionally contribute from 0.05 to 12.07 mg C m
22
d
21
to
the seafloor in the areas where we observed the remains. The sinking of
squid carcasses may constitute a significant but underestimated carbon
vector between the water column and the seafloor worldwide, because squid
populations are enormous and are regionally expanding as a result of climate
change and pressure on fish stocks. In the future, standardized methods and
surveys in geographical regions that have large squid populations will be
important for investigating the overall contribution of squid falls to regional
carbon budgets.
1. Introduction
Most deep-sea benthic communities depend on particulate organic carbon (POC)
that is synthesized in surface waters and eventually settles upon the seabed. Sedi-
ment traps have been used for decades to collect and measure this sinking
material, allowing insight into local carbon budgets [1]. Deep-sea carbon budgets
are often not closed; discrepancies exist between the amount of POC that is cap-
tured in sediment traps and the carbon required to sustain the measured biomass
and respiration of deep-benthic communities [2,3]. However, in situ observations
suggest that the remains of various megafaunal organisms and gelatinous plank-
ton, which are excluded from sediment trap analysis, may locally constitute
significant sources of carbon [4–9]. The role of medium-sized nektonic carrion
(here defined as the remains of squids, chondrichthyans and teleost fishes of
1–100 cm in length) in carbon budgets is largely unknown. Natural observations
of such carrion are so rare that typically only individual observations are pub-
lished [5,10– 12]. The paucity of observations stems from limited access to
the deep-sea habitat with the imaging tools required to observe and quantify
naturally deposited, rapidly consumed carcasses.
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Squids are opportunistic, typically fast-growing carnivores
that constitute a pivotallink between zooplankton, micronekton
and top predators [13]. They appear to be proliferating in the
ocean as a result of teleost overexploitation, warming waters
and deoxygenation [14–17]. Squids have one reproductive
cycle after which they die (semelparity) [18]. Many shallow-
water squid species aggregate to mate and to spawn, which
may locally result in high biomasses. Post-spawning mortality,
after securing egg cases to the seafloor in shallow water, results
in the deposition of squid carcasses—a phenomenon that has
been documented for neritic squid in the family Loliginidae
[19]. Squids are abundant in the open ocean and deep sea,
and carcass deposition should thus also occur in oceanic regions
where large squid populations exist. This is supported by the
fact that squid flesh can be found in the stomachs of abundant
deep-seafloor scavengers [20– 22]. Although the reproductive
behaviour of oceanic squid is poorly known, some species
(e.g. ommastrephids) aggregate for reproduction [23,24].
Nevertheless, observations of squid carrion on the deep seafloor
(greater than 200 m) are very rare; the only published account
involves carcasses of Brachioteuthis, observed off Cape Hatteras,
NC, USA, which were consumed by brittle stars and a type of
crab [23]. Scattered remotely operated vehicle (ROV) obser-
vations of post-spawning ommastrephids on the seafloor have
also occurred (M. Vecchione 2017, personal communication).
Accounts of squid carcasses at the sea surface involve spent
individuals of squid species that experience ‘gelatinous
degeneration’ [25]. The females of these species undergo
mantle tissue breakdown as a result of maturation and spawn-
ing, then float to the surface after release of the eggs [25].
There they are consumed by seabirds and other epipelagic
oceanic scavengers [25]. Various lines of evidence suggest that
postspawning dead squid also transport carbon to seafloor
communities in the deep sea, but in the absence of direct obser-
vations and measurements, the role of squid carrion in the
carbon cycle remains unknown. Here we report on squid food
falls on the deep seafloor of the Gulf of California, Mexico.
2. Results
Between February and April of 2012 and 2015, the Monterey
Bay Aquarium Research Institute conducted surveys in the
deep basins of the Gulf of California using their ROV Doc Rick-
etts. Squid carcasses and the remains of squid egg sheets were
observed on the seafloor during the course of 11 ROV dives (of
a total of 80 dives that reached the bottom) (see: http://mbari.
org/squid-carrion-images). Nine squid carcasses were encoun-
tered, at depths from 1246 to 1698 m, during six of the 11 dives
(figure 1; electronic supplementary material, table S1). Recent
carcass deposition was indicated by the fact that the mantles
of several individuals were still purple due to expanded chro-
matophores, while the arms were white (figure 1; http://
mbari.org/squid-carrion-images). Average mantle length of
squid carcasses was 351 +57 mm (range 281 –452 mm: n¼7)
(for measurements and estimations, see electronic supplemen-
tary material, SM1). A black, elongated mass was in close
proximity to six of the observed squid. Close-up imagery and
sample collection showed that these masses were hatched-
out egg sheets (figure 1). Gonatid squids brood their young
by holding darkened sheets with embedded developing
embryos in their arms [26]. Fragments of egg sheets (without
squid) of up to 540 mm in length were observed between
1072 and 3016 m depth (electronic supplementary material,
table S1). Some locations had multiple fragments, and we sus-
pect that some of these fragments came from the same egg
sheet (as indicated in electronic supplementary material,
table S1). Overall, we examined 55 individual squid food fall
locations based on the observed egg sheet fragments (see:
http://mbari.org/squid-carrion-images). Some of the food
fall locations were more than 450 km apart (electronic sup-
plementary material, table S1). While ROV bottom surveys
were performed in relatively shallow (less than 1000 m), inter-
mediate (1000– 2000 m) and deep (greater than 3000 m)
regions, most squid remains (62 remains) were found during
nine dives in waters between 1072 and 1698 m. The maximum
number of observed squid remains encountered during a
single dive included five squid carcasses and 31 egg sheet
remains (electronic supplementary material, tables S1 and
S2). The two dives that encountered the highest numbers and
densities of squid remains were at the same location (latitude
(a)
(b)
(c)
Figure 1. In situ ROV observations of living squid and squid carrion in the
Gulf of California. (a) Brooding gonatid squid (mantle length approx. 25 cm,
1100 m, dive 344; 24.48N– 109.98W). (b) Dead squid with hatched-out egg
mass with seastars (Nymphaster diomedeae) and lithodid crab Paralomis mul-
tispina (1246 m, dive 344; 24.48N – 109.98W). (c) an isolated empty squid
egg sheet (length 50 cm, 1615 m, dive 368, 26.68N –1118W). The laser
dots in (a) and (c) are 29 cm apart.
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24.408N, longitude 109.888W, in the Cerralvo Trough) in 2012
and in 2015. During ROV dives in the water column, brooding
squid (figure 1) were observed and three collected specimens
of younger ontogenetic stages were identified as Gonatopsis
octopedatus or a closely related species (R. E. Young 2012,
personal communication), suggesting that the dead squid
on the seafloor could belong to this species. Fauna observed
in the vicinity of, or scavenging on, these food falls included
Enteropneusta, Ophiuroidea, Holothuroidea, Decapoda
and Asteroidea (figure 1; electronic supplementary material,
table S1). A ratfish, Hydrolagus melanophasma, was observed
with a roughly 150 50 mm piece of carrion in its mouth
just 150 m from a squid carcass.
3. Discussion
The animal groups that were associated with the squid carcasses
have been observed at other natural food falls [27]. Conversely,
we did not observe grenadier fishes, isopods, zoarcids, liparids
or hagfish—scavengers that are reported to be abundant at arti-
ficial and natural food falls [5,11,27]. While all observed squid
carcasses and the remains of some hatched-out egg sheets had
scavenging fauna associated with them, the majority of the
latter did not, suggesting that this material is less palatable.
Gonatid squid appear to incorporate ink in the egg sheets
[28], which may act as a deterrent to some organisms, including
microbiota [29], thus increasing the time it takes to be con-
sumed. The longer residence time of egg sheet remnants
allowed us to trace back to already-consumed squid, assuming
that for each sheet a spent female squid reached the seafloor.
The 64 occurrences of squidand egg sheets are to our knowl-
edge the largest number of natural deep-sea food falls of
medium-sized nekton reported to date (electronic supplemen-
tary material, table S1). Smith [10] reported 12 food falls in the
Catalina Basin, of which eight may have had a pelagic origin.
Roper & Vecchione [23] reported two presumably spent bra-
chioteuthid squid on the seafloor, which were consumed by
brittle stars and a crab. These authors state that ‘spent, dying
squids that sink to the bottom could provide a significant
source of energy to the deep benthic fauna’ ( p. 59).
We estimate that the average observed carcass, excluding
egg sheets, of 351 mm mantle length (n¼7; see also electronic
supplementary material, SM1) weighs 1.9 kg [30]. Assuming a
scavenging rate of 5 kg d
21
[5,31], such a carcass would take
an average of 9 h to be consumed. However, Collins et al. [31]
also report that in three of nine experimental squid falls, the
bait remained untouched and in two experiments little of the
bait was consumed within the experimental period. Therefore,
9 h may be an underestimate, and squid may lie longer on the
seafloor. In any case, provided the rarity of observations in the
literature, our encounters with these food falls were likely fortu-
nate, and there is potential for high squid carcass turnoveron the
seafloor in certain areas of the Gulf of California. The high con-
centration of squid remains in some areas (up to 0.023 m
22
)also
suggests a regional abundance of these food falls, but the
absence of carcass observations during the majority of the
dives indicates heterogeneity in their deposition. Additionally,
we encountered remains more than 450 km apart, supporting
the notion that this carbon input is not limited to just one
basin within theGulf of California. The finding of squid remains
in two separate years between February and April suggests an
annual event that is spread over at least three months, but
whether or not the deposition of squid carcasses is a continuous,
episodic or seasonal process remains a matter of speculation.
Our data allowed careful estimations of the role of squid
carcass deposition in local carbon budgets. If we assume that
for each egg sheet, a squid carcass was also deposited, then
the density of carcasses would be 0–0.023 m
22
for a single
dive location (electronic supplementary material, table S2).
Assuming that the pulse of carcasses is an annual event, the
carcasses could locally contribute from 0.05 to 12.07 mg C
m
22
d
21
to the deep seafloor in the areas where they were
observed (electronic supplementary material, SM1 and table
S2). Estimates of POC flux to the deep seafloor greater than
1000 m in the Gulf of California are absent, to our knowledge.
Published records of POC flux measured by sediment traps in
the Guaymas Basin, Gulf of California at 475 m ranged from 2
to 58 mg POC m
22
d
21
(mean ¼21 mg POC m
22
d
21
) [32]. A
direct comparison would suggest that squid food falls may
locally contribute the equivalent of 0.2–57.4% of the mean
annual sediment trap flux. However, we should emphasize
that (i) the measured POC flux from sediment traps is from
shallower depths than the observed squid remains, and (ii)
the squid food fall calculations are based on individual dives
and squid carcasses were observed on only some of the benthic
dives (11 of 80 dives). Our estimated values of carbon associ-
ated with the carcasses of what is probably a single squid
species are locally relatively high. They exceed estimates for
other nekton food falls [5,10], but they are less than estimates
for certain gelatinous zooplankton species [4,6,8]. Our esti-
mations may be conservative because our calculations are
based on female squid only while male squid are also semel-
parous. Also, we have assumed that the observed carcasses
were the only carcasses deposited in that area that year (i.e.
not taking into account scavenging rates), while deposition
must occur more often. Our estimate of the area observed by
the ROV may be conservatively large, meaning that the density
may be higher than our current measurements. Finally, our cal-
culations only included the carbon associated with the squid
bodies and the squid bodies presumed to have been deposited
with the egg sheets, but not the hatched-out egg sheets them-
selves. An overestimation of our calculated flux could result
if the squid have a lower body mass than estimated here,
because female squid mobilize nutrients from their mantle
and digestive gland to fuel the long brooding time [26,28].
Also, it is possible that in some cases the squid associated
with the egg sheet observed on the sediment was consumed
by benthopelagic predators before it reached the seafloor.
Finally, it is possible that some of the egg sheet fragments
observed in the Cerralvo Trough originated from the same
squid, while we counted them as separate food falls. The
Gulf of California is a suitable area to investigate the role of
nektonic carrion in benthic carbon budgets and future research
efforts should focus on performing standardized survey
studies using in situ observations.
These first quantitative estimates of squid carrion in the
deep sea and the associated scavenging fauna suggest that
sinking squid could be an important local source of carbon,
but this source is currently not taken into account in carbon
budgets. By feeding intensively on mesopelagic prey [33],
and through high growth and metabolic rates [34], gonatid
squid very efficiently capture carbon that is stored in meso-
pelagic communities, including myctophids, which comprise
some of the largest fish biomasses on the planet [35]. As they
descend to meso- and bathypelagic depths for reproduction
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and subsequent death, gonatids, and probably other squids,
transport carbon from the epi- and mesopelagic layers to the
deep seafloor. This pathway circumvents the conventional
carbon pump concept of passively sinking particles, and results
in rapid transportation of carbon to the deep sea [22]. Our
results shed light on a process that is probably of global impor-
tance, and one that further links the largest habitats on the
planet, the deep seafloor and the pelagic realm. Squid popu-
lations worldwide are massive, supporting large industrial
fisheries [36]. Annually, sperm whales alone are estimated to
consume as much squid as all human fisheries combined
[37]. Because of the single reproductive cycle, and the typically
short lifespan of squids, populations may provide the deep sea
with annual pulses of carbon worldwide, as suggested from
the diets of abundant deep-sea scavengers [20– 22]. The
squid-associated carbon flux is probably also dynamic. Squid
populations respond flexibly and in some cases positively to
regional environmental change [15– 16]. Together with overex-
ploitation of fishes, this has resulted in a trend observed in
different marine systems where cephalopods are proliferating
[17]. Such potential ecosystem shifts probably change the
squid-associated carbon flux to the seafloor and may locally
result in an alteration of the ocean carbon pump.
Ethics. Our study is mostly based on deep-sea video observations. The
three ROV-captured squid specimens were flash-frozen at 280 C,
and subsequently defrosted and preserved in formalin for preser-
vation and examination. The expedition ‘MBARI’s 2012 Gulf of
California Expedition, R/V Western Flyer.’ (Cruise no. F2011-068)
was approved by the Mexican government via permits CTC/
001340 (from La Secretaria de Relacione Exteriores) and H00/
INAPESCA/DGIPPN/831 (Secretaria de Agricultura, Ganaderia,
Desarrollo Rural, Pesca Y Alimentacion). The expedition ‘2015 R/V
Western Flyer Gulf of California Expedition.’ (Cruise no. F2014-075)
was approved by the Mexican government via permits CTC/
01700/15 (La Secretaria de Relacione Exteriores) and DGOPA-
02919/14 (Secretaria de Agricultura, Ganaderia, Desarrollo Rural,
Pesca Y Alimentacion).
Data accessibility. The data are made available in electronic supplemen-
tary material, tables S1 and S2. ROV track coordinates on which the
distances (d) calculated in electronic supplementary material, SM1
are based and the images of food falls can be found at http://
mbari.org/squid-carrion-images.
Authors’ contributions. H.J.T.H. conceived of the study, designed the
study, helped collect the field data, analysed the data and drafted
the manuscript. S.L.B. helped collect the field data, analysed the
data and helped to draft the manuscript. S.H.D.H. and B.H.R. col-
lected field data and helped to draft the manuscript. All authors
gave final approval for publication.
Competing interests. We have no competing interests.
Funding. Financial support for this study came from the David and
Lucile Packard Foundation (H.J.T.H., S.L.B., B.H.R., S.H.D.H.), the
Monterey Bay Aquarium’s support of S.L.B., the Netherlands Organ-
ization for Scientific Research (NWO) through a Rubicon grant (no.
825.09.016) to H.J.T.H. and by a grant (CP1218) to H.J.T.H. of the
Cluster of Excellence 80 ‘The Future Ocean’. ‘The Future Ocean’ is
funded within the framework of the Excellence Initiative by the
Deutsche Forschungsgemeinschaft (DFG) on behalf of the German
federal and state governments.
Acknowledgements. We thank the MBARI ROV pilots and MBARI’s
video laboratory for their help with collecting, accessing and analys-
ing the ROV video and data. We thank Mariah Salisbury (MBARI) for
making the website with data and images. Two reviewers improved
the manuscript from its original version. Drs Ivo Bobsien and Bas
Hofman are thanked for their help with GIS.
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