Journal of Plankton Research Vol.18 no.9pp.l675-1683, 1996
Age and growth of planktonic squids Cranchia scabra and
Liocranchia reinhardti (Cephalopoda, Cranchiidae) in epipelagic
waters of the central-east Atlantic
Alexander Arkhipkin
Atlantic Research Institute of Marine Fisheries and Oceanography
(AtlantNIRO), 5 Dm.Donsk.oy Street, Kaliningrad 236000, Russia
Abstract. Statolith microstructure was studied in two abundant planktonic cranchiids, Cranchia
scabra (56 specimens, 38-127 mm mantle length, ML) and Liocranchia reinhardti (34 specimens,
99-205 mm ML) sampled in epipelagic waters of the western part of the Gulf of Guinea (tropical
Atlantic). Growth increments were revealed in ground statoliths of both species. It was possible to distinguish two growth zones in statolith microstructure by their colour in reflected light of the microscope: the translucent postnuclear zone and pale white opaque zone. Assuming that growth increments
in statoliths were produced daily, ages of the largest immature Cscabra and L.ranhardti were 166 and
146 days, respectively. Both cranchiids are fast-growing squids with growth rates in length resembling
those of juveniles of tropical ommastrephids and Thysanoteuthis rhombus. Liocranchia reinhardti
grows fasten its growth rate in ML is approximately twice that of same-aged Cscabra.Thc life cycle of
both cranchiids consists of two phases. During their epipelagic phase, Oscabra and Lreinhardti feed
and grow rapidly from paralarvae to immature young in the epipelagic waters, attaining 120-130 and
170-200 mm ML by ages of 4-5 months, respectively. Then they change their life style to a deepwater
phase.
Introduction
Cranchia scabra (Leach, 1817) and Liocranchia reinhardti (Steenstrup, 1856) are
among the most numerous squids in epipelagic waters of the open tropical Atlantic (Clarke, 1966; Arkhipkin etal., 1988; Arkhipkin and Schetinnikov, 1989). Both
squids belong to the family Cranchiidae which contains planktonic squids having
large coelomic cavities. These cavities are filled with neutrally buoyant ammoniacal fluid of low density (Denton et al., 1969) enabling squids to 'soar' in the water
column and to move using predominantly rapid flappings of small fins (Clarke,
1962).
Despite high abundance and important roles of Cscabra and L.reinhardti in the
oceanic food webs of the tropical Atlantic (Voss, 1980), little is known about the
biology of these two species. However, their morphology and anatomy (particularly that of Cscabra) are rather well studied (see Pfeffer, 1912; Naef, 1923 and
others). Both species belong to the subfamily Cranchiinae, characterized by the
presence of tubercles running from the funnel-mantle fusion onto the mantle. In
Cscabra, some of the large tubercles have an odd shape like a complex Maltese
cross (Dilly and Nixon, 1976). Paralarvae, juveniles and immature adults of
Cscabra and L.reinhardti (up to 150-157 mm of mantle length, ML) occur mainly
in epipelagic and upper mesopelagic waters (0-500 m depth), whereas mature
adults are believed to live and spawn in deep water (Clarke, 1966; Nesis, 1987).
To date, statolith microstructure in cranchiids has been studied only in a small
number of species belonging to another subfamily,Taoninae: in the Antarctic Galiteuthis glacialis (Jackson and Lu, 1994) and in the boreal Pacific Galiteuthis phyllura and Belonella borealis (Arkhipkin, 1996). It has been revealed that these
© Oxford University Press
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A-AAhlplrin
squids grow rapidly in length during the first 8-10 months of their juvenile phase
in the mesopelagic layers prior to migration into deeper waters. Age and growth
of Cscabra and L.reinhardti remain unknown.
The aim of this study was to estimate age and growth rates of Cscabra and
L.reinhardti during the epipelagic phase of their life cycle, based on statolith
microstructure analysis.
Method
Cranchia scabra and L.reinhardti were sampled in the central-east Atlantic by the
research vessel 'Ocher' in August-October 1988. Sampling localities covered open
waters of the western part of the Gulf of Guinea (latitudes 2°15'N-3o30'S and
longitudes 4°05'-15°W) off the Exclusive Economic Zones of African countries.
Squids were caught at night (20^0-04:00) at depths of 25-300 m using a Russian
zoological pelagic trawl RT/TM 33 type (vertical opening 8-10 m) equipped with
a 6 mm mesh liner. Squids were identified by the key of Nesis (1987). Dorsal mantle
length was measured in fresh squids to the nearest 1 mm. Maturity stages were
assigned from the scale developed for ommastrephid squids (Zuev et al., 1985).
Statoliths were removed from 56 specimens of Cscabra (38-127 mm ML) and
34 specimens of L.reinhardti (99-205 mm ML) aboard ship and stored in oil-paper
envelopes in 96% ethanol. Preparation of statoliths was carried out at the Laboratory of Commercial Invertebrates of AtlantNIRO using statolith-ageing techniques (Arkhipkin, 1991). Terminology of statolith parts and microstructure was
after Qarke (1978) and Lipinski etal. (1991). Total statolith length was measured
using 'MBS-10' Zoom microscope (X 32). One statolith from each pair was randomly chosen for subsequent grinding and polishing. Each statolith was first
attached with the anterior (concave) side up onto the microscopic slides with
Protexx mounting medium. After drying (usually in 24 h), statoliths were ground
on a wet waterproof sandpaper (1000 grit) and polished on a fine sandpaper (1500
grit). The partially ground statolith was then carefully extracted from the medium,
re-mounted with the posterior (convex) side up and ground again. Ground sections were embedded in Canada balsam. Growth increments were examined and
counted from the nucleus to the edge of the dorsal dome by two observers using
the eye-piece micrometer of a 'Biolam-R14' light microscope ( X 400) (Arknipkin,
1991). If the statolith was overground, the other statolith from the same specimen
was prepared. Growth increments were visible and countable in all statolith
preparations. The total number of growth increments for each statolith was taken
as a mean of two replicate counts if the deviation between the two counts was less
than 5%. If the deviation was more than 5% (as in seven statoliths of Cscabra and
five statoliths of L.reinhardti), those statoliths were re-counted once more by the
same two observers. After re-counting, the deviation between two counts became
less than 5% in all statoliths.
Growth increments of Cscabra and L.reinhardti were well-resolved and resemble those of the ommastrephid squid IUex illecebrosus (Dawe et al., 1985). The
validation of daily deposition of statolith growth increments has been confirmed
for the post-embryonic period in a number of squid species (reviews: Lipinski,
1676
Growth of pUnktonk (quids
1993; Jackson, 1994). Therefore, I assume that the hypothesis 'one day - one
growth increment' is true also for Cscabra and Lreinhardti. Thus, the total
number of growth increments within their statoliths was believed to represent age
of squid in days. Hatching dates were back calculated. Linear function was fitted
to the age-at-length data in Cscabra only for further estimation of daily growth
rates (DGR, mm or g per day) and instantaneous rate of growth (G). The values
of both ML and B W were calculated for each 20-day interval using the formula of
the best fitted curve. DGR and G were calculated after Ricker (1958) as:
= (W2-W1)/T,
G = (lnW2-\nWl)/T,
where W\ and Wl are calculated ML or BW values at the beginning and end of
the time interval (T= 20 days).
There was not enough data for estimation of these parameters in L.reinhardti
due to a rather narrow size range of specimens studied.
Results
Statolith microstructure and growth
Statolith microstructure in Cscabra and L.reinhardti is quite similar between
species (Figures 1 and 2). The focus lies under the spur of the statolith. There is a
small (1-2 urn) dark-brown (calcium?) concretion in the centre of the ovoid
nucleus. In Cscabra, the maximum diameter of the nucleus is significantly larger
(range 20-32.5 um, mean 25.8 urn, SD = 2.45) than that of Lreinhardti (range
17.5-27.5 um, mean 21.6 um, SD = 2.54).
It was possible to distinguish two growth zones in the statolith microstructure
by their colour in reflected light of the microscope. The inner, postnuclear zone
was translucent, whereas the outer, dark zone is pale white. However, in transmitted light it was impossible to distinguish clearly the boundary between these
zones due to a practical absence of any stress check or a sharp change in increment width (Figures 1 and 2).Thus, the number of growth increments was not estimated within each zone. Around the nucleus, growth increments were narrow
(2.5-3 um) and fairly visible. In the dark zone of the statolith, the width of growth
increments gradually increased up to 5-6 um, then decreased to 3-4 um near the
statolith margin (Figures 1 and 2). No checks were observed within the statolith
microstructure of either species.
In Cscabra, the largest relative sizes of statoliths were observed in a juvenile of
38 mm ML (1.57% ML), the smallest in immature females of 108 and 127 mm ML
(0.88%). In L.reinhardti, relative sizes of statoliths were less than in Cscabra. In
the smallest specimen (an immature female of 99 mm ML), statoliths were 0.8%
ML, whereas in the largest immature female (205 mm ML) statoliths were only
0.4% ML.
In Cscabra, allometric growth of the total statolith length (versus mantle
length) is negative with rather high value of the coefficient '6' (0.519,Table I).
1677
A.Arkhrpkirj
• * V ' "•L--**•-••-*?Fv*. •'•?•&<• * t
AT*f*i
Fig. L Light mkrophotographs of the statolith of Cscabra (immature female, ML 113 mm). (A)
Nucleus (N), postnuclear zone (PZ), and dark zone (DZ); (B) dark zone near the statolith margin.
Scale bar = 50 jun.
Squid age and growth
The youngest Cscabra (40 mm ML) had 72 growth increments within the statolith,
while the youngest L.reinhardti (a male of 134 mm ML) had 94 statolith growth
increments. The oldest Cscabra (two immature females of 114 and 118 mm ML)
had an age of 166 days, whereas the oldest L.reinhardti (an immature male of 183
mm ML) had only 146 growth increments.
The length-at-age data in Cscabra were fitted by a linear function (Figure 3,
Table I). Sexual dimorphism in sizes of the same-aged animals was not revealed.
At the same ages, L.reinhardti is approximately two times larger in length than
Cscabra (Figure 3A). Although a shortage of data has not allowed the sexual
dimorphism in length of L.reinhardti to be estimated, it seems that males tend to
be larger than the same-aged females (Figure 3A).
During the ontogenetic period of Cscabra studied, the ML DGR were constant,
0.75 mm day-1 (Figure 3B). Instantaneous rates of growth in ML decreased gradually (Figure 3B). Taking into account larger sizes of the same-aged Lreinhardti,
both DGR and G in ML are obviously higher in this species than in Cscabra.
In samples investigated, all squids were immature. Females could be
1678
Growth of pbnktonic squids
Fig. 2. Light microphotographs of the statolith of Lrcinhardti (immature male, ML 134 mm). (A) Dark
zone near the statolith margin; (B) nucleus (N) and postnuclear zone (PN). Scale bar = 50 jim.
distinguished by the presence of two stripe-like nidamental glands on the ventral
surface of the coelom, whereas males were identified by an oval primordium of
the spermatophoric gland on the right side of the coelom. The gonad was paletransparent in both sexes. However, in one male of L.reinhardti (205 mm ML) the
testis and spermatophoric gland were pale-white. Based on back-calculated hatching dates, examined specimens of Cscabra and L.reinhardti hatched between
April and June of 1988 (Figure 4).
Discussion
Formation of growth zones within statolith microstructure seems to be characteristic for squids. Usually, these zones are distinguishable by increment width and
especially, by colour in coldwater oceanic and neritic species, like Gonatus fabricii
Table L Cranchia scabra. Relationships between total statolith length in mm (STL); mantle length in
mm (ML).
Power growth curve: STL versus ML
Linear function: age versus ML
Parameter
Estimate
a
b
a
b
0.09123
0.5194
-10.76
0.7495
Standard .
error
0.014414
0.03492
11.05
0.06331
0.8382
0.7218
Parameters of the power (allometric) function Y = a-X1", and linear function Y = a + b-X, their standard errors and /{-squares.
1679
AjiikhipUn
zou°
I 200-
A
Cr f
" * •
a
Cr m
g>150
*
Uf
-
+
Lim
+
*
+
5 100§
00
00
20
40
60 80 100 120 140 160 180 200
Number of increments
0.018.C
80
0.002JT
100 CO 140 WO 180 200
Number of Increments
Fig. 3. (A) Relationship between number of growth increments (age) and mantle length in males (m)
and females (f) of Oscabra (Cr) and L.reinhardti (Li). (B) Daily growth rates and instanteneous rates
of growth in Qscabra.
(Gonatidae) (Kristensen, 1980),Illex illecebrosus (Morris and Aldrich, 1984), Illex
argentinus (Arkhipkin, 1990) (Ommastrephidae). In warmwater oceanic species,
the 'dark' zone is pale and visible mainly in reflected light [Sthenoteuthis pteropus
(Arkhipkin and Mikheev, 1992); Enoploteuthis leptura (Arkhipkin, 1994)]. Tropical-subtropical shelf species like Ioliginids have an almost translucent 'dark zone'
[Loligo vulgaris (Arkhipkin, 1995)], and usually the microstructure of their statoliths has not been divided into growth zones at all (Jackson and Choat, 1992;
Jackson, 1994).Tropical cranchiids Qscabra and L.reinhardti are not an exception
to the rule: growth increments within their statoliths can be grouped into growth
zones. However, in contrast to other tropical oceanic species (S.pteropus, EJeptwa,
op.cit) which have three growth zones within their statoliths, Qscabra and L.reinhardti have only two zones: postnudear and opaque (dark) ones. Jackson (1993)
suggested that a transition between the inner opaque (dark) and outer translucent
(peripheral) growth zones in Moroteuthis ingens (Onychoteuthidae) (this squid
does not have a translucent postnudear zone within the statolith) may relate to a
1680
Growth of planktonk squids
100
80
C.scabra
L.reinhardti
5 60
c
|
4020 0
F
M
A
M
Hatching month
J
J
A
Fig. 4. Hatching dates of Cranchia scabra and Liocranchia reinhardti in 1988.
possible ontogenetic shift of this squid from shallow to deepwater habitat. It is
likely that the translucent peripheral zone within statoliths of Cscabra and L.reinhardti develops later, after their shift to deep water.
It is notable that there is not a check at the boundary between the postnuclear
and opaque zones in statoliths of both cranchiids studied. This fact indirectly indicates that their food capture apparatus does not transform during a transition
from paralarval to juvenile phases, causing a short-term starvation and formation
of a 'stress' mark in the statolith, like in ommastrephids (Arkhipkin and Mikheev,
1992). This has been confirmed by morphological studies of arm and tentacle
development in cranchiids (Pfeffer, 1912; Naef, 1923).
Cranchia scabra and L.reinhardti are among the fast growing squids in the
epipelagic waters of the tropical Atlantic. At the same ages, growth rates in mantle
length of Cscabra resemble those of S.pteropus juveniles (Arkhipkin and Mikheev,
1992). Moreover, at an age of 150 days, Lreinhardti has somewhat lesser mantle
length than the fastest-growing squid of the tropical epipelagic waters, Thysanoteuthis rhombus (Nigmatullin et al., 1995). However, growth rates in weight of
both cranchiids having a quite thin and transparent mantle are likely to be much
less than those of nektonic squids having thick and muscular mantle and fins.
It is suggested that tropical cranchiids spawn at great depths (Nesis, 1985). It is
likely that just after hatching, small paralarvae ascend to epipelagic waters. This
fact has been confirmed by captures of very small paralarvae (3.3 mm ML in
Cscabra and 2.4 mm ML in L. reinhardti, respectively) in the superficial water
layer of the open tropical Atlantic (Arkhipkin et al., 1988). During the first 4-5
months of their ontogenesis, Cscabra and Lreinhardti feed and grow quickly in
the epipelagic waters, attain 120-130 and 170-200 mm ML, respectively, and then
move into deep water for maturation and subsequent spawning. Unfortunately, a
lack of mature animals in my samples (presumably occurring at great depths) does
not allow estimation of the longevity of both cranchiids. Future investigations of
deepwater bathyal fauna of the open ocean could clarify this problem.
Both high abundance and fast growth rates of Cscabra and L.reinhardti juveniles show that these cranchiids successfully co-exist with abundant oceanic
1681
A.AiUiipkin
oramastrephids and utilize to a considerable extent the food resources of the
epipelagic waters in the tropical Atlantic.
Acknowledgements
I am grateful to A.B.Mikheev for statolith sampling. Comments of Dr A.Guerra
(IIM, Vigo, Spain) and an anonymous referee helped to improve the manuscript.
The research described in this publication was supported in part by the International Science Foundation and Russian Government under Grant No. NNF300.
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Received on December 21,1995; accepted on April 9,1996
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