New data on the life history and ecology of the deep-sea hooked squid Taningia danae

Abstract

Three specimens of Taningia danae were captured in the northern Spanish (eastern Atlantic) waters in late 2000. The total weights of the animals, two females and one male, were 66, 124 and 19 kg, respectively. Both females were maturing with no trace of eggs in the oviduct. The potential fecundity of the largest female was close to 5 million oval-shaped oocytes ranging from 0.4 to 1 mm. This female represented the heaviest record of T. danae to date. A description of the first mature male of this species is also undertaken. The reproductive strategy adopted by this species seems to rely on multiple spawning. The most remarkable feature of the male was the presence of a long penis with a total length of 73 cm that protruded 23 cm beyond the mantle. The number of growth increments in the statoliths was 647 and 1052, for each female, respectively. Assuming that these growth increments are deposited daily, the estimated age of these specimens would be 21 and 33 months, respectively. Remains of the blue whiting Micromesistius poutassou, some exoskeleton fragments of crustaceans and small hooks of Gonatus sp. were present in their stomach contents. The geographical and vertical distribution and the possible influence of water temperature and upwelling events on the growth of this species are discussed.

Full text

New data on the life history and ecology of the deep-sea hooked squid Taningia
danae
A. F. Gonza´lez, A. Guerra & F. Rocha
Gonza´ lez AF, Guerra A, Rocha F. 2003. New data on the life history and ecology of the deep-sea
hooked squid Taningia danae.Sarsia 88:000–000.
SARSIA
Three specimens of Taningia danae were captured in the northern Spanish (eastern Atlantic) waters in
late 2000. The total weights of the animals, two females and one male, were 66, 124 and 19 kg,
respectively. Both females were maturing with no trace of eggs in the oviduct. The potential fecundity
of the largest female was close to 5 million oval-shaped oocytes ranging from 0.4 to 1 mm. This female
represented the heaviest record of T. danae to date. A description of the first mature male of this species
is also undertaken. The reproductive strategy adopted by this species seems to rely on multiple
spawning. The most remarkable feature of the male was the presence of a long penis with a total length
of 73 cm that protruded 23 cm beyond the mantle. The number of growth increments in the statoliths
was 647 and 1052, for each female, respectively. Assuming that these growth increments are deposited
daily, the estimated age of these specimens would be 21 and 33 months, respectively. Remains of the
blue whiting Micromesistius poutassou, some exoskeleton fragments of crustaceans and small hooks of
Gonatus sp. were present in their stomach contents. The geographical and vertical distribution and the
possible influence of water temperature and upwelling events on the growth of this species are
discussed.
A. F.Gonza
´lez*, A. Guerra & F. Rocha, Instituto de Investigaciones Marinas, Eduardo Cabello 6,
ES-36208 Vigo, Spain
E-mail: afg@iim.csis.es
*Corresponding author
Keywords: Cephalopods; Taningia danae; ecology; life history.
INTRODUCTION
The oceanic squid Taningia danae Joubin, 1931 has
been found throughout the world’s oceans (Roper &
Vecchione 1993). This octopoteuthid squid is a
cosmopolitan species, mainly found in tropical, sub-
tropical and, to a lesser extent, boreal waters (Nesis
1987). The most remarkable external features of this
species are the presence of two rows of hooks on the
arms, the lack of tentacles in adult specimens, the
presence of two very large photophores in the tips of
arms number two and the oval shape of the large, broad
fins. This squid is reported to be oceanic and meso-
pelagic and probably spawns in deep waters, but its
biology is poorly known (Roper & Vecchione 1993).
The majority of the specimens analysed world-wide,
including most large ones, were found in the stomach
contents of predators, principally sperm whales,
although a few have also been taken from the stomachs
of sharks, lancetfishes, tunas, wandering albatross and
elephant seals (Roper & Vecchione 1993). Taningia
danae reaches 57°N in the northeastern Atlantic (Santos
& al. 2001), but it has been recorded mostly in the
stomach contents of sperm whales off Spain (Clarke &
MacLeod 1974). Fishing gears tend to collect the
smallest specimens, while sperm whales capture the
bigger ones. Until this report, the heaviest fished T.
danae on record weighed 61.4 kg (Roper & Vecchione
1993). The largest specimen found in the stomach of a
sperm whale was a squid with a mantle length (ML) of
1490 mm (Okutani & al. 1976).
The aim of the present paper is to provide biological
and ecological data of three large T. danae fished in the
Carrandi fishing ground (northern Spanish Atlantic
waters) in late 2000. We also describe the largest male
and the heaviest individual caught to date. A description
of the reproductive system of females and males of this
species is given for the first time.
MATERIAL AND METHODS
Three specimens of T. danae were caught alive on the
Carrandi fishing ground (43°52.54'N05°18.74'W). The
pair trawler Boer collected the animals in mid-water at
about 400–600 m depth on 20 September 2000 (speci-
men 1), 30 October 2000 (specimen 2, Fig. 1A) and on
20 December 2000 (specimen 3, Fig. 1B). Wet weights
were recorded before freezing. The reproductive
systems and statoliths (specimens 1 and 2) were
removed for further studies. All animals were fixed in
SARSIA (Taylor & Francis) J:/SARSIA/71/MS71.3D Page Count: 6
FULL TEXT SGML :: Ms: 71 Op: MJW/f1 Cycle: PGW/F2-PDF On: 22/08/2003 At: 14:49:54 Page 1 (1 - 6)
DOI 10.1080/00364820310002524 #2003 Taylor & Francis
Published in collaboration with the University of Bergen and the Institute of Marine Research, Norway

4% formalin and later preserved in 70% ethanol. They
are now lodged in the Museo Aula del Mar in Luarca
(Spain).
Morphometric measurements were made according
to Roper & Voss (1983). Beak measurements follow
Clarke (1986). We included a new measurement,
photophore length of the right number two arm.
Statoliths of specimens 1 and 2 were removed and
measured to the nearest 0.01 mm. Statoliths were
mounted in Crystalbond
1
resin. Both sides of the
statolith were ground to reveal growth increments using
30 mm carborundum paper for grinding and 3 mm for
polishing. The growth increments in statoliths were
counted using a semiautomatic image analysis system
(TNPC 3.0
1
) employing a high-resolution digital
camera (Sony DCR-PC11E) mounted on a compound
microscope (Nikon OPTIPHOT-2). Video images made
at 200 magnification were then processed with the
computer program TNPC 3.0
1
. Counts were made
along transects extending outward from the nucleus
(underneath the dorsal dome) to the rostrum.
A sample of 1.074 g, from three different parts of the
ovary (proximal, medial and distal), was obtained from
specimen 2 to estimate total potential fecundity. Oocyte
major axis length was measured to the nearest 0.1 mm
using a binocular microscope equipped with a measure-
ment reticule and the total number of oocytes of all
sizes present in the subsample was determined. The
resulting size frequency was then appropriately scaled
to estimate the total present in the whole 617 g ovary.
Stomach contents were separated into fish, cephalo-
pods and crustaceans. Fish were identified from
vertebrae and scales by reference to Watt & al.
(1997). Cephalopods were identified from beaks
(Clarke 1986) and hooks.
RESULTS
The three captured squid weighed 66 kg (1050 mm ML;
specimen 1), 124 kg (1320 mm ML; specimen 2) and
19 kg (1190 mm ML; specimen 3). Specimen 2 is the
heaviest fished T. danae ever observed world-wide and
specimen 3 is the first fully mature adult male reported
to date. The morphometric measurements are summar-
ized in Table 1. The arms had the characteristic two
rows of hooks and all the squid lacked tentacles. The
mantle was thick (20 mm in specimen 2 and 12 mm in
specimen 3) and gelatinous.
Both females were maturing with small oocytes in
the ovary, but no eggs were present in the oviduct. The
potential fecundity of specimen 2 was close to 5 10
6
oocytes. The size of the oval-shaped oocytes was
normally distributed and ranged from 0.4 to 1.0 mm,
with an average maximum length of 0.64 0.13 mm.
No trace of implanted spermatophores was found.
The male reproductive tract was composed of testis,
spermatophoric gland, Needham’s sac and penis. The
most remarkable feature of this mature male was its
730 mm long penis situated on the right side of the
mantle cavity, which protruded 230 mm beyond the
mantle. Two spermatophores were found in the penis.
The smaller one measured 54 mm in total length and
was intact, while the larger one was 166 mm in total
length and was open at its distal end. The longest
spermatophore looked like an empty tubule with sperm
Fig. 1. A. The heaviest Taningia danae ever captured (124 kg).
B. The male specimen showing the long penis protruding
outside the mantle.
SARSIA (Taylor & Francis) J:/SARSIA/71/MS71.3D Page Count: 6
FULL TEXT SGML :: Ms: 71 Op: MJW/f1 Cycle: PGW/F2-PDF On: 22/08/2003 At: 14:50:17 Page 2 (1 - 6)
2Sarsia 88:1-6 – 2003

attached near its broken end. Furthermore, a large
quantity of sperm was also found inside the penis.
The statolith length of specimen 1 was 3.11 mm and
the statolith width was 2.16 mm. The statolith length and
width of specimen 2 were 3.24 and 2.36 mm, respec-
tively. The number of growth increments in the statoliths
was 647 for specimen 1 and 1052 for specimen 2.
Assuming daily periodicity in the deposition of growth
increments, the estimated age for specimens 1 and 2
would be 21 and 33 months, respectively.
Two stomachs (specimens 1 and 3) contained food
remains. The stomach of specimen 1 contained a lower
mandible, vertebrae and scales of the blue whiting
Micromesistius poutassou, some integuments of crus-
taceans, a lower beak of Gonatus sp. (5 mm lower
rostral length), two hooks of 8.5 mm and other small
hooks (2–3 mm) resembling hooks of the tentacular
club of Gonatus sp. The stomach of specimen 3
contained only three vertebrae of Micromesistius
poutassou.
DISCUSSION
Although the presence of T. danae in northern waters of
the eastern Atlantic has been inferred from beaks and
specimens found in whale stomachs, none had been
caught by commercial fishing or research vessels until
recently (Santos & al. 2001). This is surprising given
the heavy fishing activity conducted throughout the
eastern North Atlantic and the large increase in
biological sampling activities in that area over the past
30 years.
Roper & Vecchione (1993) cautiously suggested that
small specimens of T. danae occur close to the surface up
to 100 m depth, while larger specimens could live at
depths attaining 1250 m. However, Santos & al. (2001)
reported that a tiny juvenile (32 mm ML) was captured in
a net fishing 800 m deep. Our specimens were collected in
mid-water at a depth ranging from 400 to 600 m. These
findings agree with the vertical distribution of adult T.
danae previously reviewed by Roper & Vecchione
(1993). Our observations of two maturing females and
a fully mature male in mid-water indicate that this species
is not continuously associated with the bottom, a question
that also intrigued [AQ1] Nesis (1996). However,
maturing females and fully mature males of many bottom
gonatid squids such us Berryteuthis magister may be
regularly caught in mid-water, but the fully mature
females are caught only near the bottom. Thus, the
catches of maturing females and mature males of T.
danae in mid-water do not contradict the supposition of
bottom-spawning (Nesis, pers. comm.).
As both females had oocytes in all stages of maturation
with a dominant population, it appears that ovulation is
group synchronous. Females of this species appear to be
sexually mature over a broad size range. Clarke (1967)
reported on two mature females: the smaller one was only
71 cm ML, while the larger one was almost double in size
at 1400 mm ML. Such a broad size-at-maturity range and
a group synchronous ovulation suggest that T. danae is
more likely to be a multiple spawner than an intermittent
terminal spawner. This spawning pattern is found in
relatively stable environments such as in the deep sea
(Rocha & al. 2001). The large difference in potential
fecundity between the two females examined and
Clarke’s 1400 mm ML specimen, 5 10
5
eggs, may
Table 1. Measurements (mm), weight (kg) and counts of the
specimens of Taningia danae collected in the Carrandi fishing
ground according to Roper & Voss (1983) and Clarke (1986).
Specimen
1
Specimen
2
Specimen
3
Sex F F M
Maturity stage II–III II IV
Total length 1850 2030 1190
Mantle length 1050 1320 700
Total weight 66 124 19
Mantle width 290 350 240
Head width 230 320 190
Fin length 103 1290 –
Fin width 940 1170 560
Eye diameter 99 105 72
Gill length 980 1290 700
Nidamental gland length 230 420 –
Arm length
L1 425 660 270
L2 430 530 320
L3 480 500 290
L4 395 490 295
R1 435 – –
R2 440 – 290
R3 500 – –
R4 405 – 290
Arm hook count
L1 640 680 640
L2 520 520 –
L3 640 580 –
L4 560 560 720
R1 640 – –
R2 520 – –
R3 680 – –
R4 560 – 460
Photophore length 72 76 30
Funnel cartilague length 82 150 65
Funnel cartilague width 43 72 30
Funnel length 190 230 155
Free funnel length 76 80 60
Penis length – – 730
Penis width – – 35
Spermatophore length – – 54 & 166
Upper beak rostral length 25 23 –
Lower beak rostral length 24 26 –
SARSIA (Taylor & Francis) J:/SARSIA/71/MS71.3D Page Count: 6
FULL TEXT SGML :: Ms: 71 Op: MJW/f1 Cycle: PGW/F2-PDF On: 22/08/2003 At: 14:50:18 Page 3 (1 - 6)
Gonza
´lez & al. – New data on the deep-sea squid Taningia danae 3

either reflect that Clarke counted only mature eggs or,
more simply, that larger squid produce more eggs. Aside
from the obvious presence of the male’s protruding penis,
the external appearance of both sexes is the same. We did
find a clear difference in size between sexes: the
immature females were much larger than the mature
male.
Some oceanic squids have slight modifications of
some arms or no hectocotylus at all. They introduce the
sperm into wounds produced by their beaks or hooks as
in the case of Onychoteuthidae, Gonatidae, Chiroteuthi-
dae, Mastigoteuthidae and Architeuthidae (Okutani &
Ida 1986; Nesis 1987; Norman & Lu 1997). Consider-
ing the lack of a hectocotylized arm and the presence of
a long penis in our mature male, it seems that
reproduction in T. danae could be similar. We did not
observe wounds in the mantle of the females, probably
because our specimens were not quite fully mature.
The advanced state of digestion of the blue whiting
found in both specimens precludes the possibility that
the whiting were ingested while in the net. The remains
of Gonatus could be either G. fabricii or G. steenstrupi.
Because the geographical distribution of G. steenstrupi
includes the Bay of Biscay (Nesis 1987), it is likely that
the remains belong to the latter species.
Until now, the largest captured specimen was the
mature female caught in the northwest Atlantic that
measured 1600 mm ML and 61 kg reported by Roper &
Vecchione (1993). Zeidler (1981) reported the capture
of three dead T. danae floating at the surface, and the
heaviest animal he collected weighed 110 kg. There-
fore, our specimen 2 represents the heaviest reported T.
danae.
Wood & O’Dor (2000) concluded that coleoid
cephalopods achieve larger size by delaying maturity
and that temperature, as well as phylogeny, must be
considered when making interspecific comparisons.
They postulated that larger size at maturity is a
consequence of longer life-spans rather than faster
growth rates. This appears to be the case for the
specimens analysed, if we assume daily deposition of
growth increments. Although there is no information
about paralarvae of T. danae, the oocyte size
(0.4–1.0 mm) of the maturing females suggests that the
paralarvae would have a similar size at hatching of other
cephalopods with similar oocyte size, i.e. Illex coindetii
(Gonza´lez & Guerra 1996). Therefore, the instantaneous
relative growth rate (G) for T. danae at maturity would be
1.64 and 1.70 for specimens 1 and 2, respectively.
The annual sea surface temperature in the Carrandi
fishing ground varies from 12 to 19 °C (AVHRR
satellite data), while the water temperature between 200
and 400 m depth ranges from 11 to 12 °C (Rı´os & al.
1987). The high weights at maturity attained by our
specimens are quite similar to those observed in other
large cephalopods (e.g. Octopus dofleini) that live in
cold water (Hartwick 1983). Taningia danae and
Octopus dofleini also have low G (1.64 and 1.31,
respectively) for similar temperature ranges. However,
in northern Spanish waters, other squids attain higher G
values and have shorter life-spans over the same
temperature range, which indicates that much of the
difference in life-span is unlikely to be related to
temperature. Therefore, intrinsic physiological factors
allow some cephalopod species to live longer and attain
larger sizes.
Although the relationship between size and age at
maturity in cephalopods is unknown, one of the possible
factors that affect this relationship may be related to
resource availability (Atkinson & Sibly 1997). Squids
seem to be limited by predators rather than by
availability of prey, because they usually live in high
production areas (Wood & O’Dor 2000). In the
Carrandi fishing ground, wind-driven upwelling of
eastern North Atlantic central water during the summer
near the coast causes blooms of phytoplankton (Botas
& al. 1988). Simultaneously, organic matter and
sediments are exported offshore from the continental
margins during these upwelling periods (Ferna´ndez &
al. 1993). These two processes lead to increased
secondary production characterized by a high abun-
dance of pelagic and benthic vertebrates and inverte-
brates. The high abundance of zooplankton supports
important fish populations (principally the blue whiting,
Micromesistius poutassou) that serve as prey for T.
danae and giant squids such as Architeuthis [AQ2]
(Gonza´lez & al. in press).
Overall, the results of this paper support the conclu-
sion of Wood & O’Dor (2000) who observed that
coleoid cephalopods attain larger size by delaying
maturity and that temperature must be considered when
analysing growth rates and when making interspecific
comparisons. The bottom topography, the oceanogra-
phy of the area and the existence of important
communities of marine fishes suitable as prey suggest
that the Carrandi fishing ground is a favourable habitat
for these ‘giant squids’.
ACKNOWLEDGEMENTS
We thank Mr Luis Laria and CEPESMA and the crew of the
pair trawler Boer for providing the specimens. We are also
indebted to Dr Kir N. Nesis who kindly reviewed this
manuscript. We also thank Mrs M
a
Teresa Ferna´ ndez and Mr
Joaquı´n Gracia for their technical assistance.
SARSIA (Taylor & Francis) J:/SARSIA/71/MS71.3D Page Count: 6
FULL TEXT SGML :: Ms: 71 Op: MJW/f1 Cycle: PGW/F2-PDF On: 22/08/2003 At: 14:50:19 Page 4 (1 - 6)
4Sarsia 88:1-6 – 2003

REFERENCES
Atkinson D, Sibly RM. 1997. Why are organisms usually
bigger in colder environments? Making sense of a life
history puzzle. Trends in Ecology and Evolution
12:235–239.
Botas JA, Bode A, Ferna´ndez E, Anado´n R. 1988. Descripcio´n
de una intrusio´ n de agua de elevada salinidad en el
Canta´ brico central: distribucio´ n de los nutrientes
inorga´ nicos y su relacio´n con el fitoplancton. Investiga-
cio
´n Pesquera 52:561–574.
Clarke MR. 1967. A deep-sea squid, Taningia danae Joubin,
1931. Symposium of the Zoological Society of London
19:127–143.
Clarke MR. 1986. A handbook for identification of cephalopod
beaks. Oxford: Clarendon Press. 273 p.
Clarke MR, MacLeod N. 1974. Cephalopod remains from a
sperm whale caught off Vigo, Spain. Journal of the
Marine Biological Association UK 54:959–968.
Ferna´ ndez E, Cabal J, Acun
˜a JL, Bode A, Botas A, Garcı´a-Soto
C. 1993. Plankton distribution across a slope current-
induced front in the southern Bay of Biscay. Journal of
Plankton Research 15:619–641.
Gonza´ lez AF, Guerra A. 1996. Reproductive biology of the
short-finned squid Illex coindetii (Cephalopoda,
Ommastrephidae) of the northeastern Atlantic. Sarsia
81:107–118.
Gonza´ lez AF, Guerra A, Rocha F, Gracia J (In press). Recent
findings of the giant squid Architeuthis in northern
Spanish waters. Journal of the Marine Biological
Association UK.[AQ3].
Hartwick B. 1983. Octopus dofleini. In: Boyle PR, editor.
Cephalopod life cycles: species accounts, Vol. 1.
London: Academic Press. p 277–292.
Nesis KN. 1987. Cephalopods of the world; squids, cuttlefishes
and allies. Neptune, NJ: TFH Publications. p 1–351.
Norman MD, Lu CC. 1997. Sex in giant squid. Nature
389:683–684.
Okutani T, Ida H. 1986. Rare and interesting squid in Japan –
IX. A mass occurrence of Chaunoteuthis mollis
Appello¨ f, 1891 (Oegopsida: Onychoteuthidae) from
off Japan. Venus 45:53–60.
Okutani T, Satake Y, Ohsumi S, Kawakami T. 1976. Squids
eaten by sperm whales caught off Joban District, Japan
during January–February, 1976. Bulletin of the Tokai
Regional Fisheries Research Laboratory 87:67–113.
Rı´os AF, Fraga F, Figueiras FG, Prego R, Pe´ rez FF. 1987.
Campan
˜as oceanogra´ ficas “Asturias I, II, III y IV”.
Datos Informativos del Instituto Investigaciones
Marinas, Vigo 22:1–140.
Rocha F, Guerra A, Gonza´lez AF. 2001. A review of the
reproductive strategies in cephalopods. Biological
Reviews 76:291–304.
Roper CFE, Vecchione M. 1993. A geographic and taxonomic
review of Taningia danae Joubin, 1931 (Cephalopoda:
Octopoteuthidae), with new records and observations
on bioluminescence. In: Okutani T, O’Dor RK, Kubo-
dera T, editors. Recent advances in fisheries biology.
Tokyo: Tokai University Press. p 441–456.
Roper CFE, Voss GL. 1983. Guidelines for taxonomic
descriptions of cephalopod species. Memoirs of the
National Museum of Victoria 44:49–63.
Santos MB, Pierce GJ, Gonza´lez AF, Santos F, Va´zquez MA,
Collins MA. 2001. First records of Taningia danae
(Cephalopoda, Octopodidae) in Galician waters (NW
Spain) and in Scottish waters (United Kingdom).
Journal of the Marine Biological Association UK
81:355–356.
Watt J, Pierce GJ, Boyle PR. 1997. A guide to the premaxillae
and vertebrae of North Sea fishes. ICES (Co-operative
Research Report) 220:1–231.
Wood JB, O’Dor RK. 2000. Do larger cephalopods live
longer? Effects of temperature and phylogeny on
interspecific comparisons of age and size at maturity.
Marine Biology 136:91–99.
Zeidler W. 1981. A giant deep-sea squid, Taningia sp., from
South Australian waters. Transactions of the Royal
Society of South Australia 105:218.
Accepted 14 June 2002 – Printed ?? ????? 2003
Editorial responsibility: Jarl Giske
SARSIA (Taylor & Francis) J:/SARSIA/71/MS71.3D Page Count: 6
FULL TEXT SGML :: Ms: 71 Op: MJW/f1 Cycle: PGW/F2-PDF On: 22/08/2003 At: 14:50:20 Page 5 (1 - 6)
Gonza
´lez & al. – New data on the deep-sea squid Taningia danae 5

QUERIES TO BE ANSWERED BY AUTHOR (SEE MARGINAL MARKS)
IMPORTANT NOTE: Please mark your corrections and answers to these
queries directly onto the proof at the relevant place.
Do NOT mark your corrections on this query sheet
Query No. ..Query
[AQ1]..........Nesis 1996 in text, 1987 in reference list. Please clarify
[AQ2]..........Gonzalez & al. in press. Published?
[AQ3]..........Gonzalez & al. in press. Published?
SARSIA (Taylor & Francis) J:/SARSIA/71/MS71.3D Page Count: 6
FULL TEXT SGML :: Ms: 71 Op: MJW/f1 Cycle: PGW/F2-PDF On: 22/08/2003 At: 14:50:20 Page 6 (1 - 6)
6Sarsia 88:1-6 – 2003