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ORIGINAL PAPER
Growth and mating of southern African Lycoteuthis
lorigera (Steenstrup, 1875) (Cephalopoda; Lycoteuthidae)
H. J. T. Hoving ÆM. R. Lipinski Æ
M. A. C. Roeleveld ÆM. D. Durholtz
Received: 10 February 2006 / Accepted: 14 November 2006 / Published online: 23 December 2006
Springer Science+Business Media B.V. 2006
Abstract Lycoteuthis lorigera is an oceanic
squid that is abundant in the Benguela system.
Little is known about the biology of this squid
except that it is eaten in large numbers by
numerous oceanic predators and that males grow
to larger size than females, which is unique for
oegopsid squid. The aim of this study was to
better understand the biology of this species by
investigating its age and growth, as well as its
mating system. Toward this end, the age of 110
individuals, ranging from 35 to 110 mm, was
estimated by counting statolith growth incre-
ments. Estimates of age ranged from 131 to
315 days and varied with mantle length. No
significant differences were found in the size of
males and females of equivalent ages. The rela-
tionship between ML and age for both sexes was
best described by an exponential growth curve,
probably because no early life stages were aged in
this study. Only one mature male (ML 160 mm)
was aged, and preliminary estimates suggest it
was 386 days old. Instantaneous growth rates
were low (0.54% ML/day and 1.4% BM/day) but
consistent with enoploteuthid growth rates. When
the growth rate of L. lorigera was corrected for
temperature encountered during the animal’s life,
the growth rate was fast (0.47% BM/degree-days)
and consistent with the hypothesis that small
cephalopods grow fast and that large cephalopods
grow older, rather than fast. Mature females were
often mated and had spermatangia in a seminal
receptacle on the dorsal pouch behind the nuchal
cartilage. Males probably transfer spermatangia
to the females using their long second and/or
third arm pair since the paired terminal organs
open far from the mantle opening.
Keywords Lycoteuthis lorigera Growth rate
Reproduction Ageing Statoliths
Introduction
Due to the full utilisation of neritic marine
resources, the exploitation of deep-water ecosys-
tems is increasing. The collection of basic biolog-
M. A. C. Roeleveld deceased.
H. J. T. Hoving (&)
Department of Marine Biology,
University of Groningen, CEES, P.O. Box 14,
9750 AA Haren, The Netherlands
e-mail: H.J.T.Hoving@rug.nl
M. R. Lipinski M. D. Durholtz
Department of Environmental Affairs and Tourism,
Private Bag X2, Roggebaai 8012,
8000 Cape Town, South Africa
M. D. Durholtz
e-mail: Durholtz@deat.gov.za
M. R. Lipinski
e-mail: Lipinski@deat.gov.za
123
Rev Fish Biol Fisheries (2007) 17:259–270
DOI 10.1007/s11160-006-9031-9
ical data on inhabitants of deep-water ecosystems
is therefore important in designing management
plans for sustainable exploitation of these systems.
One of the most important inhabitants of these
ecosystems are squid because they form a trophic
link between epipelagic and bathypelagic ecosys-
tems, as both active predators as well as important
prey items (Clarke 1996). Currently, little is known
about the life history (age, growth and reproduc-
tion) of most oceanic squid (Nesis 1995; Wood and
O’Dor 2000; Arkhipkin 2004).
One particularly poorly understood oceanic
family of squid is the Lycoteuthidae. This family
consists of two subfamilies and four genera that
comprise a total of five described species. One
member of this family, Lycoteuthis lorigera
(Steenstrup 1875), is an abundant squid in the
Benguela ecosystem. This species dominates, in
numbers the epibenthic cephalopod fauna on the
continental slope of the South East Atlantic
between 300 and 900 m depth (Roeleveld et al.
1992). Although no current fisheries exist, the
high abundance and muscular appearance of
L. lorigera suggests that this species might be a
suitable resource for exploitation (Lipinski 1992).
L. lorigera is preyed upon by commercially
important fish, such as deep-water Cape hake,
Merluccius paradoxus, and Kingklip, Genypterus
capensis (Lipinski et al. 1992), as well as several
smaller cetacean species (Ross 1984), the Portu-
guese shark Centroscymnus coelolepis (Ebert
et al. 1992), ribbonfish Lepidopus caudatus
(Meyer and Smale 1991), the southern lantern-
shark Etmopterus granulosus (Lipinski et al.
1992) and in New Zealand waters the species is
preyed upon by petrels (Imber 1975). This species
feeds on pelagic crustaceans and fishes, including
myctophids (Voss 1962).
In spite of the abundance and the important
role of L. lorigera in the South East Atlantic
ecosystem, little is known about the biology of
this species. Clearly, this needs to be improved,
particularly as L. lorigera is a unique species
amongst the oegopsids in having males that grow
to a larger size than females. Another rare feature
for squid is the presence of paired spermatophoric
organs in males of L. lorigera. The aim of this
study is to investigate the age, growth and mating
system of L. lorigera.
The best method for estimating the age and
growth of squid is counting statolith increments.
Daily deposition of increments has been validated
for numerous species of squid, including oegops-
ids (for review see Arkhipkin 2004). Although the
daily deposition of increments has not yet been
validated for L. lorigera, it has been in the
paralarvae of the enoploteuthid Abralia trigon-
ura, which belongs to a phylogenetic sistergroup
of the Lycoteuthidae (Bigelow 1992; Young and
Harman 1998).
The lifespan of oegopsid squid has been found
to range from 3 months for the tropical Atlantic
enoploteuthid Pterygioteuthis gemmata, which
reaches an adult size of 3 cm (Arkhipkin 1997),
to 2–3 years for the large sub-tropical mesope-
lagic octopoteuthid, Taningia danae (Gonza
´lez
et al. 2003). Most deepwater oegopsid squid,
however, tend to live for a minimum of 1 year
(Arkhipkin 2004). This is longer than the 1 year
or less lifespan of myopsids (reviewed by Jackson
2004).
So far, no lycoteuthids have been aged. Given
its unique biology, it would be interesting to
determine where L. lorigera will fit on the
oegopsid longevity scale. It is generally accepted
that squid that inhabit colder waters (either polar
or deeper waters) grow slower, and for longer
(Arkhipkin 2004). To compensate for tempera-
ture differences, Wood and O’Dor (2000) intro-
duced the physiological timescale; in which
growth and longevity are corrected for temper-
ature. Taking the animals’ mean life time tem-
perature of the environment into account, species
that have a slow absolute growth rate can still
grow relatively fast. This approach will be used in
the interpretation of growth in L. lorigera.
In addition, information will be presented on the
spermatophore production, morphology of the
male reproductive apparatus and the mode of
spermatophore transfer from male to female, to
better understand the mating system of the species.
Materials and methods
An analysis of annual demersal surveys con-
ducted by the Department of Environmental
Affairs and Tourism (DEAT) of the Republic of
260 Rev Fish Biol Fisheries (2007) 17:259–270
123
South Africa using the South African research
vessel ‘‘Africana’’ and the Norwegian research
vessel ‘‘Dr. Fridtjof Nansen’’ between 1986 and
2005 provided preliminary data on the distribu-
tion of L. lorigera around South Africa. This
species was present in trawls between 192 and
1388 m deep, but was absent on the continental
shelf (Fig. 1).
L. lorigera used for ageing purpose were
collected during four research cruises in South
African and Namibian waters (Table 1). The
mantle length (ML) and body mass (BM) of
animals were measured to the nearest mm and
0.1 g respectively. The stage of sexual maturity
was determined using the method of Lipinski and
Underhill (1995). Statolith nomenclature was
after Clarke (1978). Statoliths were extracted
and stored dry. The total statolith length (TSL)
was measured to the nearest 0.01 mm.
Statoliths (Fig. 2) were sectioned frontally
through the lateral dome using the method of
Lipinski and Durholtz (1994) and polished using
polishing cloth. Sectioned statolith images were
recorded under phase contrast by an AxioCam
MRc camera mounted on a Zeiss Axioscope 40
compound microscope. A TV2/3 ‘‘C 0.63·camera
mounted magnifying lens, together with a 10·/0.25
or a 40·/0.65 objective lens, were used to produce
low and high resolution images, respectively. The
images were recorded using AxioVision Ver. 4.2
software package supplied by Carl Zeiss Vision
GmbH. A number of over-lapping high resolution
images were taken of sectors with the highest ring
clarity along transects from the nucleus, a distinct
ring around the protostatolith, to the edge of the
lateral dome (Fig. 3A). Increments were counted
from images using the counting feature of the
software. The rings in the outer part of the lateral
dome (Fig. 3B) were often obscured, and extrap-
olation (based on the increment width of approx-
imately 10 of the last countable rings) was then
used to determine the number of rings in the
periphery of the section. In order to increase
accuracy, counting the increments on every axis
was repeated five times. The mean of the separate
counts was used for that particular axis.
The instantaneous relative growth rate (G) was
calculated using the equation:
G= (lnW
2
–lnW
1
)/t, where W
1
and W
2
are
either ML (mm) or BM (g) at the beginning
and end of time interval t(Forsythe and Van
Heukelem 1987).
Wood and O’Dor (2000) introduced the phys-
iological instantaneous relative growth rate (G/
T). G= (lnW
2
–lnW
1
)/t
2
–t
1
, where W
1
is the
hatchling mass (g) and W
2
is the mass of a mature
female. t
2
–t
1
represents the age (days) at matu-
rity. Tis the average temperature encountered
15°E20
°E25
°E
35°S
30°S
25°S
Port Elizabeth
Cape Town
Fig. 1 Distribution of
L. lorigera around South
Africa. Dots indicate
presence of specimens in
trawls and the dashed line
indicates the 200 m depth
contour
Rev Fish Biol Fisheries (2007) 17:259–270 261
123
during the individual’s lifetime. G/Tis expressed
in degree-days.
In order to estimate hatching mass for L.
lorigera, a value of 80% of the egg mass was used.
The egg mass was calculated from the egg
diameters (1.1 ± 0.1 mm) obtained from eggs
from the oviduct. The eggs were assumed to be
spherical (volume 4/3pr
3
), and to have a density
Table 1 Collection details and study purpose of L. lorigera specimens used in this study
Museum no./Station no. nStudy purpose Latitude Longitude Depth (m) Collection dates Vessel
NO 2 A7613 15 ML-BM/Ageing 2704¢S1436¢E 280 16.08.1988 Africana
A24307–A24384 7 ML-BM/Ageing 30–33S15–17E 314–448 21.01.2005–02.02.2005 Africana
NA 970-021–NA 1096-147 79 ML-BM/Ageing 28–35S14–18E 392–582 10.02.2005–07.03.2005 Nansen
NA 1120, 1122, 1125 9 ML-BM/Ageing 28–35S14–18E 529–605 01.10.2005–03.10.2005 Nansen
SAM-S3709 1 ML-BM/Testis mass 3243¢S1643¢E 457 10.02.1988 Africana
SAM-S3481 1 ML-BM/Testis mass 3515¢S1841¢E Surface 08.02.1992 Africana
SAM-S2094 1 ML-BM/Testis mass 3229¢S1635¢E 390 24.06.1987 Africana
SAM-S1793 1 ML-BM/Testis mass 3448¢S1816¢E 510 06.07.1986 Africana
SAM-S1975 1 ML-BM/Testis mass 3215¢S1624¢E 425 26.06.1987 Africana
SAM-S2046 3 ML-BM/Testis mass 3326¢S1727¢E 680 05.03.1988 Africana
SAM-S2073 1 ML-BM/Testis mass 3440¢S1812¢E 447 12.03.1988 Africana
SAM-S2078 3 ML-BM/Testis mass 3438¢S1815¢E 482 14.03.1988 Africana
SAM-S3431 1 ML-BM/Testis mass 3012¢S1453¢E 488 02.08.1990 Africana
SAM-S2047 2 ML-BM/Testis mass 3319¢S1728¢E 451 06.03.1988 Africana
SAM-S789 2 ML-BM/Testis mass 351¢S18E 600 24.05.1982 Africana
SAM-S3430 1 ML-BM/Testis mass 3439¢S1804¢E 500 11.02.1992 Africana
SAM-S3436 1 ML-BM/Testis mass 3227¢S1645¢E 357 15.02.1992 Africana
SAM-S4074 1 ML-BM/Testis mass – – – – –
NA 892-036 2 ML-BM/Testis mass 2914¢S1429¢E 451 9.05.2004 Nansen
NA-911-059 1 ML-BM/Testis mass 3423¢S1748¢E 397 09.12.2004 Nansen
NA 631 1 ML-BM/Testis mass 3222¢S1629¢E 450 02.06.2003 Nansen
NA 891 5 ML-BM/Testis mass 2921¢S1429¢E 543 09.05.2004 Nansen
Fig. 2 Posterior (A)
and anterior (B) view
of respectively the left
and right statolith of
a mature female
L. lorigera
(ML = 91 mm)
262 Rev Fish Biol Fisheries (2007) 17:259–270
123
equal to the density of water (Wood and O’Dor
2000). The obtained value was compared to the
mass of eggs preserved in 70% ethanol and was
found to be realistic.
The mass of a mature female was estimated by
using the mean mass of the mature females
examined in this study (=45.1 g). The same was
done to estimate the age at maturity for females
(=299 days). Although both body mass and age
varied, this was taken as a representative figure to
estimate physiological growth rate. The average
lifetime temperature (T) was estimated to be 8C
(Shannon 1985; depth 600 m at 24S). To com-
pare the obtained results with the results of Wood
and O’Dor (2000), only the physiological growth
rate of the female was estimated.
The body mass and testis mass of 29 mature
males of L. lorigera (Table 1) were determined.
The spermatophores of three males were counted
and measured. The body mass obtained for males
was used for the ML–BM relationship because of
the absence of fresh mature males. The males
were fixed in formalin and stored in 70% ethanol.
Results
Statoliths
TSL for females was 2.25 mm (ML = 99 mm) and
2.56 for males (ML = 174 mm). The relative size
of the statoliths (% ML) decreased with increas-
ing mantle length (TSLI = –0.0185 ML + 3.932;
R
2
= 0.93).
There was no significant difference between
the TSL of males and females of similar sizes (ML
54–82 mm; TSL 1.62–1.95 lm; Student t-test:
P> 0.05: n= 7). The relationship between TSL
and the number of increments (TSL = 0.08
age
0.57
;R
2
= 0.94) indicates that the growth rate
of the statoliths slows down with size (and age) by
the deposition of smaller increments. This was
confirmed in sectioned statoliths where the incre-
ments were widest in the first 100 days of the
animal’s life, with a maximum increment width of
approximately 4 lm. Thereafter, the increment
width decreased gradually to approximately
1lm.
The nucleus was distinct in sectioned stato-
liths, with a mean maximum length of 22 lm
(SD = 2.1; n= 32; range 18.25–26.42 lm). The
increments that were closest to the nucleus had
to be counted along an axis that runs towards
the concave side of the statolith (Fig. 3A). At
the point where increments were visible in the
lateral dome, the counting axes were linked,
and counting was completed along the second
axis through the lateral dome. With the excep-
tion of one mature male in which 18% of the
axis was extrapolated, extrapolation never ex-
ceeded 12%. For over 80% of the statoliths, a
minimum of 93% of the total counting axis was
readable. The agreement between counts of
paired statoliths was good (mean differ-
ence = 2.7% ± 2.5%; n= 13), suggesting that
our counts were accurate. Because of additional
access to statoliths, another 9 statoliths of
mature females were sectioned and growth
increments were counted. Four of these stato-
liths could be completely counted and in the
other five between 93 and 98% of all incre-
ments could be read.
Fig. 3 A sectioned
statolith of a mature
female L. lorigera (ML
100 mm; 291 increments)
(A) overview of a frontal
section through the dorsal
dome and the wing (B)
Detail of the periphery of
the dorsal dome showing
narrow increments of
approximately 1 lm
Rev Fish Biol Fisheries (2007) 17:259–270 263
123
Age and growth
Mature males were almost twice as large as
mature females (Fig. 4). The allometric equations
for the relationship between BM and ML was
BM = 0.0002ML
2.72
for females and
BM = 0.0002ML
2.67
for males.
The ML of mature females ranged from 88 to
110 mm, corresponding with an age of 290–
315 days (Figs. 4,5A). The ML of (formalin
preserved) mature males ranged from 136 to
194 mm (Fig. 4). The smallest (unsexed) individ-
ual aged had a ML of 35 mm and was 131 days
old. The smallest female measured had a ML of
46 mm ML and was 152 days old, while the
youngest male measured 53 mm in ML and was
175 days old (Fig. 5A). The only mature male
(ML = 160 mm) aged was estimated to have 386
growth increments. The size range of the seven
immature males was 54–82 mm. Since the age of
males and females of equivalent size did not differ
significantly (Student t-test: P> 0.05; n= 7), it
suggested that the growth of young males is
comparable to that of females, but the males
attain a bigger overall size because they grow for
longer.
Exponential, linear and power growth curves
were fitted to the ML- and BM-at-age data, for
juveniles, females and males separately, as well as
the pooled data (Table 2). Of these curves, both
the ML-at-age and BM-at-age relationships were
best described by an exponential growth curve
(Fig. 5).
Using the exponential growth curve, the instan-
taneous growth rates for ML and BM were
calculated to be 0.54% ML/day and 1.4% BM/
day, respectively (Fig. 5).
To determine the physiological instantaneous
growth (G/T), the hatching size of L. lorigera was
estimated to be 0.00056 g while size at maturity
was taken as the mean BM of the mature females
for which age was determined (45.1 g). The mean
age a mature female was 299 days. Assuming
an average life time temperature of T=8C
(Shannon 1985; 600 m of depth), it was estimated
that these females had an instantaneous relative
growth rate (G) of 3.8% BM/day and a physio-
logical instantaneous relative growth rate (G/T)
of 0.47% BM/degrees-day. The Gcalculated here
is different from the earlier fitted growth curve
because it is based on only two data points: the
size at hatching and the size at maturity.
Spermatophore transfer
The male reproductive system consists of a small
testis and a small spermatophoric organ with a
short terminal organ. Testis size varied between
19 and 55 mm in length and a maximum width of
2–9 mm. The largest testis mass of L. lorigera was
0.6 g (Fig. 6). There seemed to be a gradual
increase in testis mass with mantle length, up to a
0
50
100
150
200
250
300
0 50 100 150 200 250
ML (mm)
BM (g)
Juveniles (n=42)
Immature females (n=58)
Mature females (n=26)
Immature males (n=26)
Mature males (n=27)
Immature males (pres.) (n=2)
Fig. 4 Mantle length–
body mass relationship
for male, female and
juvenile L. lorigera. Note
that the values for mature
males are based on
formalin preserved
specimens
264 Rev Fish Biol Fisheries (2007) 17:259–270
123
ML of 165 mm when testis mass decreased, most
probably due to the production and transfer of
spermatophores.
The terminal organ ranged from 28 to 37 mm
in large mature males, with the exception of
17 mm in a mature male of 136 mm ML, and
opened under the gill between 65 and 50 mm
from the mantle margin. The lining of the
terminal organ was transparent, with the sperma-
tophores visible through the lining. The sperma-
tophores were situated with their aboral end
toward the opening of the terminal organ.
Spermatophores were typified by a short coiled
sperm mass (10–28% TSL) and a cement body
(32–57% TSL) that were attached laterally to the
sperm reservoir. The length of the ejaculatory
y = 19.524e0.0054x
R = 0.9496
2
0
20
40
60
80
100
120
0 50 100 150 200 250 300 350
No. of increments
ML (mm)
Females
Males
Juveniles
y = 0.648e0.0143x
R = 0.941
2
0
10
20
30
40
50
60
70
0 50 100 150 200 250 300 350
No. of increments
BM (g)
Females
Males
Juveniles
A
B
Fig. 5 Growth curve of
pooled data (A) ML—no.
of statolith increments
(B) BM—no. of statolith
increments
Rev Fish Biol Fisheries (2007) 17:259–270 265
123
apparatus varied between 30 and 40% TSL.
Spermatophore length was 8.0–12.6 mm in a male
of 186 mm ML, and 9.0–11.0 mm in a small
mature male of 136 mm ML.
An interesting feature of the reproductive
system of male L. lorigera was the presence of
paired spermatophoric and terminal organs.
These paired organs were both functional, as
spermatophores were found in both terminal
organs. The number of spermatophores in the
packed terminal organs of three males did not
vary significantly within individuals (130 and 135;
54 and 55; 126 and 132 spermatophores in the
right and left organ, respectively). However, in a
small mature male (ML 136 mm) the left terminal
organ contained 14 spermatophores, while the
right spermatophoric organ and terminal organ
were not fully developed. In addition, 25 sperma-
tophores containing no sperm were found in the
left terminal organ, while the right terminal organ
was empty in a presumably spent male (ML
176 mm, BM 142 g).
Females possessed a specialised pouch for
receiving the spermatangia, the seminal recepta-
cle. The opening of the seminal receptacle was
situated dorsally in the midline, where the mantle
and the visceral sac fused, directly behind the
posterior end of the nuchal cartilage (Fig. 7). The
organ was only visible when the anterior 40 mm
of the dorsal mantle, including gladius, were
removed. The receptacle was approximately
10 mm long and had a maximum width of 4 mm
at the opening, and had rugose walls. Inside the
receptacle, a bundle of 10–15 spermatangia were
found, adherent to each other, and the bundle
occupied the whole lumen. Approximately
1–2 mm of the aboral ends of the spermatangia
was protruding from the receptacle. The cement
bodies of the spermatangia could be seen as
reddish bodies at the oral end of the bundle,
which was situated at the posterior end of the
receptacle.
The paired oviducts of 10 mature females
contained between 721 and 3798 ova. The max-
imum diameter of the ova measured
1.1 ± 0.1 mm (n= 10).
Table 2 Values for growth curves fitted for pooled and separate data for L. lorigera
ML— no. of increments BM— no. of increments
ab R
2
abR
2
n
Juveniles Linear function 0.3125 –3.7393 0.6321 0.1187 –12.668 0.6557 27
Power function 0.174 1.0997 0.6529 1.00E-06 3.043 0.6957
Exponential function 15.18 0.0069 0.6429 0.2777 0.0193 0.6939
Males Linear function 0.2515 7.3067 0.857 0.1594 –19.55 0.8696 9
Power function 0.6041 0.8606 0.8378 2.00E-04 2.1335 0.8483
Exponential function 26.736 0.0038 0.8517 1.847 0.0095 0.8535
Females Linear function 0.3982 –22.599 0.9025 0.3276 –54.421 0.8235 74
Power function 0.0754 1.2532 0.9041 6.00E-07 3.178 0.8845
Exponential function 19.752 0.0053 0.9226 0.8044 0.0135 0.8967
All Linear function 0.3605 –13.139 0.9285 0.2678 –39.16 0.8415 110
Power function 0.1289 1.1557 0.9385 9.00E-07 3.0897 0.9393
Exponential function 19.524 0.0054 0.9496 0.648 0.0143 0.941
Number of animals for which the no. of increments was determined is indicated as n. Linear function: y=ax +b; power
function: y=ax
b
; exponential function: y=ae
bx
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0 50 100 150 200 25
0
Mantle len
g
th
(
mm
)
Testis mass (g)
Mature males
Immature males
Fig. 6 Testis mass and ML relationship for immature and
mature male L. lorigera
266 Rev Fish Biol Fisheries (2007) 17:259–270
123
The nidamental gland length of 64 females
increased with the onset of maturity. The glands
of stage I females were 4.3 ± 1 mm (n= 15) in
length, while those of stage II, III, IV and V were
8 ± 1.1 mm (n= 21), 18.5 ± 0.7 mm (n= 2),
20.7 ± 2.5 mm (n= 6) and 27.6 ± 4 mm
(n= 20), respectively.
Discussion
Age and growth
A strong relationship was found between body
mass and mantle length for both males and
females. There was little variation in size at
maturity for females, with the smallest mature
female measuring 84% of the ML of the largest
female. In comparison, the smallest mature male
measured 70% of the ML of the largest male.
L. lorigera exhibits a strong sexual size dimor-
phism (SSD), with males attaining almost twice
the size of females (ratio ML
max
$/#= 0.54). Male
biased sexual size dimorphism is common in the
neritic squid family Loliginidae, but is unknown
for oegopsids (Nesis 1987). This gives rise to the
idea that there are common ecological or evolu-
tionary forces acting on body size in males and
females in both L. lorigera and loliginids. Male
biased SSD generally occurs when there is strong
male to male competition, female preference for
large male size (sexual selection), or when there is
trophic dimorphism (Fairbairn 1997).
Growth increments in the statoliths of
L. lorigera were well resolved but extrapolation
was often necessary to estimate final age. All the
mature females aged in this study were 315 days
old or younger, suggesting that their lifespan is
one year or slightly less. In contrast, the one
mature male we had access to was estimated to be
more than a year old (386 days). This estimate,
however, should be considered preliminary be-
cause 18% of its age was extrapolated. Neverthe-
less, it suggests that males of this species probably
live longer than females.
The relationship between BM and age for
squid between 35 and 105 mm ML was best
described by an exponential growth curve. How-
ever, this curve is unlikely to adequately describe
the growth of this species entire ontogenesis. A
recent comparison of growth curves to describe
cephalopod growth found that the exponential
growth curve was the best fit for only the two
smallest sample sizes (early life history stages
were underrepresented) in a study of 12 species of
squid. The overall best result was obtained when
the Schnute curve was fitted, a 4 parameter
sigmoid growth curve (Arkhipkin and Roa-Ureta
2005). It is likely that the lack of individuals
<35 mm ML and greater than 110 mm ML is
biasing our attempts to adequately describe
growth. Unfortunately, squid of these sizes are
proving extremely difficult to catch.
One objective in this study was to get an idea
of the growth rate of L. lorigera and compare it
with other squid species in the same ontogenetic
stage and size class. For this reason, Gwas
calculated from the fitted exponential growth
curve to the obtained age at size data. Although
the instantaneous growth rates of 0.54% ML/day
and 1.4% BM/day were low, they were similar
to those reported for the enoploteuthid squid
Fig. 7 Dorsal view of the mantle of a preserved mature
female L. lorigera (ML = 100 mm) showing the opening of
the seminal receptacle (SRO), the nuchal cartilage (NC)
and the cement bodies (CB) of the spermatangia. A
triangular part of the mantle has been removed to show
the seminal receptacle
Rev Fish Biol Fisheries (2007) 17:259–270 267
123
Abraliopsis pfefferi (Arkhipkin 1996) in their
mature ontogenetic phase. Such similarities in
growth rates might be explained by the fact that
lycoteuthids and enoploteuthids are phylogenetic
sistergroups (Young and Harman 1998).
Based on the instantaneous growth rate (sensu
Wood and O’Dor (2000)) of 3.8% BM/day of
L. lorigera, it is a slow growing squid. However,
when this value is corrected for temperature, the
physiological instantaneous growth rate (G/
T= 0.47% BM/degree-days) of L. lorigera is
higher than the growth rates presented for any
of the teuthids examined by Wood and O’Dor
(2000).
The physiological relative instantaneous
growth rate and size at maturity found for L.
lorigera correspond with the trend found by
Wood and O’Dor (2000) for several other cole-
oids. There is a negative correlation between
physiological relative instantaneous growth rate
and size at maturity, implying that small cepha-
lopods grow faster and that large cephalopods
grow older, rather than faster. There seems to be
a life history trade-off in squid between maturing
early at a small size and maturing later at a large
size, where fitness is increased by a short period
between hatching and maturity for fast growing
small squid. On the other hand, larger squid have
a higher fecundity, which also increases fitness
(Wood and O’Dor 2000). The low instantaneous
growth rate for L. lorigera, and the contrasting
high physiological instantaneous growth rate,
show that life for some oceanic squid may appear
slow, but when corrected for the low temperature
these species encounter compared to neritic
squid, life for oceanic squid is fast.
Mating system
Besides size, additional sexual dimorphic charac-
ters of the males are the extreme elongation of the
second and third arm pair. Villanueva and
Sanchez (1993) have studied these features in
detail, stating that the first and fourth arm pairs do
not show hectocotylisation in L. lorigera, but that
the second and third arm pairs show extreme
elongation and modification. The modification of
the third arm pair accounts for one third of the
total arm length. Although Forch and Uozumi
(1990) suggested modification of the fourth arm
pair, they added that this might be due to sucker
loss or regeneration. A general rule in the repro-
ductive systems of squid seems to be that species
that lack a hectocotylus have a long muscular
terminal organ, which is used in the transfer of
spermatophores (Nesis 1995). The terminal organs
of L. lorigera are very short, and protrude from
under the gills, about 50–65 mm from the mantle
opening. Nesis (1995) mentioned that the short
terminal organs in L. lorigera probably indicate
functional immaturity, and the organs should grow
much longer towards functional maturity. We do
not agree with that, because spent males were
found with empty spermatophores and short
terminal organs. Without a long muscular termi-
nal organ, a hectocotylus or specialised arm is
necessary for the transfer of spermatophores to
the female. The elongated and modified arm pairs
two and three described by Villanueva and San-
chez (1993) are therefore very likely to play a role
in spermatophore transfer. Additionally, the sym-
metry in both the elongation of arm pairs two and
three and the terminal organs may be another clue
that supports transfer of spermatophores using the
long arms.
Males exhibit a strong decline in testis mass,
and probably continuation of growth after reach-
ing maturity. The reduction of testis mass is
caused by the use of sperm for the production of
spermatophores, which is generally an irrevers-
ible process. Such reduction in testis mass is also
seen in spent males of the deepwater squid
Moroteuthis ingens, a terminal spawner (Jackson
and Mladenov 1994).
Paired spermatophoric complexes are rare in
squid. The only other squid that share this devel-
opment with L. lorigera are Histioteuthis hoylei,
Selenoteuthis scintillans and Lycoteuthis springeri
(Nesis 1982; from Arkhipkin 1992), the latter two
being members of the same family as L. lorigera.
Both male organs of L. lorigera contained sperma-
tophores, indicating that they were both functional.
Comparing the number of spermatophores in the
terminal organ and the number of spermatangia in
mated females indicates that males are capable of
mating with several females.
The seminal receptacle is here described for
the first time. The position of the organ is similar
268 Rev Fish Biol Fisheries (2007) 17:259–270
123
to that of pyroteuthids (Young and Harman
1998). The organ has a small opening and it is
plausible that the males use their modified long
arm pairs two and/or three for the deposition of
spermatangia into the seminal receptacle. Long,
thin arms would be able to grasp the spermato-
phores from the opening of the terminal organ
that is situated quite deep in the mantle cavity.
Furthermore, the thin arms could be of use in
depositing the spermatangia into the small open-
ing of the seminal receptacle.
Acknowledgements Management and staff of Marine
and Coastal Management (DEAT), Iziko Museums of
Cape Town and the Institute of Marine Research in
Bergen, Norway, are thanked for their support. Richard
Laubscher is thanked for initial help with statolith
preparation and reading. Mr. Mandilese Mqoqi is
thanked for collection of specimens. Drs. Deniz Haydar
is thanked for help with illustrations and English language.
Drs. Dick Young is thanked for help with determining the
position of the described seminal receptacle. This research
was partly financed by the Schure-Beijerinck-Popping
Fonds (KNAW-Royal Dutch Academy for Science), the
Dr. Hendrik Muller’s Vaderlandsch Fonds and Stichting
Fundatie van de Vrijvrouwe van Renswoude.
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