Iteroparity or Semelparity in the Jumbo Squid Dosidicus gigas: A Critical

Choice
Authors: Vladimir Laptikhovsky, Alexander Arkhipkin, Marek R. Lipiński, Unai Markaida,
Hilario Murua, et. al.
Source: Journal of Shellfish Research, 38(2) : 375-378
Published By: National Shellfisheries Association
URL: https://doi.org/10.2983/035.038.0218

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 Journal of Shellfish Research, Vol. 38, No. 2, 375–378, 2019.

ITEROPARITY OR SEMELPARITY IN THE JUMBO SQUID DOSIDICUS GIGAS:

A CRITICAL CHOICE

VLADIMIR LAPTIKHOVSKY,1* ALEXANDER ARKHIPKIN,2 MAREK R. LIPIŃSKI,3

UNAI MARKAIDA,4 HILARIO MURUA,5 CHINGIZ M. NIGMATULLIN,6
WARWICK H. H. SAUER3 AND HENK-JAN T. HOVING7
1
Centre for Environment, Fisheries and Aquaculture Science, Pakefield Rd., Lowestoft NR33 0HT,
United Kingdom; 2Falkland Islands Government Fisheries Department, Bypass Rd., P.O. Box 598,
Stanley FIQQ 1ZZ, Falkland Islands; 3Department of Ichthyology and Fisheries Science, Rhodes
University, P.O. Box 94, Grahamstown 6140, South Africa; 4El Colegio de la Frontera Sur, CONACyT,
Av. Rancho Polı́gono 2-A, Campeche 24500, Mexico; 5AZTI Tecnalia, Herrera Kaia, Portualde z/g,
Pasaia 20110, Spain; 6Atlantic Research Institute of Fisheries and Oceanography (AtlantNIRO), Dm.
Donskoy St., 5, Kaliningrad 236000, Russia; 7GEOMAR, Helmholtz Centre for Ocean Research Kiel,
Düsternbrooker Weg 20, Kiel 24105, Germany

ABSTRACT The jumbo squid Dosidicus gigas was recently claimed to be an iteroparous species with ovaries returning to an
immature, resting stage after spawning. Analysis of the data and figures presented in two recent articles revealed that this claim
was based on misinterpretation of histological information and that Dosidicus is not iteroparous. Having consensus on the
reproductive strategy of Dosidicus is important for the management of fisheries for this species.

KEY WORDS: Dosidicus gigas, jumbo squid, oogenesis, iteroparity, reproduction

Recently, two articles on the reproductive biology of the semelparous species (sensu Cole 1954) such as Anguilla or
large nektonic jumbo squid Dosidicus gigas (d
Orbigny, 1835) Oncorhynchus. In other species (polycyclic or iteroparous) this
(Ommastrephidae) have been published: Hernández-Muñoz cycle occurs repeatedly every few years or every year’’ (Kamler
et al. (2016) and Pérez-Palafox et al. (2019). Both studies 1992). Cephalopods generally do not live for many years, and in
present a nearly identical claim of finding postovulatory follicles their case, the ‘‘semelparous species’’ simply implies that each
(POF) in immature females of D. gigas. Based on their findings, animal during ontogenesis has only one reproductive cycle, and
it was stated that D. gigas should be considered as iteroparous after the single spawning period, they die (Rocha et al. 2001).
and that the ovary of this squid is subject to several cycles of The ovary of adult ‘‘iteroparous species’’ of cephalopods, after
maturation, spawning, and consequent recovery, with the go- the first complete reproductive cycle, is then subjected to several
nad returning to the immature stage after each spawning phase. sequential reproductive cycles, and the reproductive system
If so, to our knowledge this would be a first case of iteroparity in reverts to the immature condition after each spawning period
oegopsid squids. Here, reasons why this claim is unfounded are (Nigmatullin 2002, 2015). This condition was found in
discussed. Vampyroteuthis infernalis (Hoving et al. 2015) and its possibility has
Currently, there is some uncertainty in the definitions used been suggested for Kondakovia longimana (Laptikhovsky et al.
when describing reproductive strategies in cephalopods. This is 2013).
largely due to the fact that there are two kinds of interpretation An alternative point of view was expressed by Rocha et al.
of parity in reproductive strategies. One considers the number (2001) who criticized the semelparity–iteroparity concept be-
of reproductive cycles or breeding opportunities in the life his- cause of the wide array of reproductive strategies found in
tory, and the other considers the number of spawning activity cephalopods. Rocha et al. (2001) differentiated strategies be-
events (i.e., repeatability of egg release) during each re- tween spawning once based on the ovary monocyclicity and
productive cycle or spawning season (Murua & Saborido-Rey spawning more than once based on either monocyclicity (most
2003). Lamont Cole, who introduced the terms ‘‘semelparous’’ cephalopods) or polycyclicity (Nautilus).
and ‘‘iteroparous,’’ wrote: ‘‘. Some organisms are Following the aforementioned interpretations of iteroparity
semelparous, that is to say, they reproduce only once in a lifetime .. and semelparity in cephalopods, the main conclusion of the
iteroparous forms, . those which reproduce more than once studies by Hernández-Muñoz et al. (2016) and Pérez-Palafox
in a lifetime.’’ (Cole 1954, p. 105), thus not stating anything et al. (2019) is challenged, which, based on the presence of
about the repeatability of spawning events. The modern con- a resting gonadal phase, described Dosidicus gigas as a
sensus, however, is that the terms monocyclic reproduction and polycyclicity/iteroparous species.
semelparous are synonyms, as is the case for the terms poly- Histological and morphological examination of oogenesis
cyclic reproduction and iteroparous (Murua & Saborido-Rey has been performed for several genera of ommastrephid squids,
2003). For example, in fish: ‘‘in some species such a [gonad] including Illex (Laptikhovsky & Nigmatullin 1992, Lin et al.
cycle occurs only once before death; these are monocyclic or 2017), Sthenoteuthis (Burukovsky et al. 1977, Laptikhovsky &
Nigmatullin 2005), Todarodes (Hamabe 1963, Nigmatullin &
*Corresponding author. E-mail: [email protected] Laptikhovsky 1994), Ornithoteuthis (Arkhipkin et al. 1998),
DOI: 10.2983/035.038.0218 and Dosidicus gigas (Ochoa-Báez 1982, Arkhipkin 1992,

375
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 376 LAPTIKHOVSKY ET AL.

Markaida 2001, D ı́az-Uribe et al. 2006, Nigmatullin & (Fig. 6 a–d in Pérez-Palafox et al. 2019); however, their ‘‘POF’’
Markaida 2009). The overall conclusion of these studies was were actually sections of blood vessels (see Figure 1 in Lum
that ommastrephids do not exhibit ovarian polycyclicity. Once Kong 1993) with attached primary oocytes subjected to atresia
the ommastrephid gonad has reached the mature condition and (see Figure 3b in Melo & Sauer 1998). In the figure caption, it
produces ripe eggs, it never returns to the immature condition was stated that ‘‘The postovulatory follicles are formed by fcs
but continues to produce yolk oocytes until the ovary is spent [follicular cells] supported by connective tissue constituted by
and enters into a regressing phase. During this single period of reticular or collagenous elastic fibers when dyed blue, indicating
ovary maturation, the reproductive system itself might be sub- that they are collagen fibers.’’ This, in fact, is a description that
jected to cycles of spawning events expressed in periodical perfectly fits a typical composition of animal blood vessels, in-
replenishing and emptying of the oviducts during the pro- cluding those of squids (Shadwick 1999). The ‘‘POF’’ described
duction of pelagic egg masses. This spawning cyclicity may in Pérez-Palafox et al. (2019) look rather different from ‘‘real’’
happen in squids with intermittent or continuous spawning POF, as described in Hernández-Muñoz et al. (2016) Figure 1,
because of asynchronous maturation of individual oocytes panel 8, and which were well described for Loligo reynaudii
resulting in spawning of the eggs in different batches. In squids (Melo & Sauer 2007).
with synchronous oocyte maturation, the oviducts are filled and The degeneration of POF takes less than 48 h (often less than
emptied just once in the life cycle. Examples of the latter include 24 h) in subtropical and temperate squids and fish spawning at
deep-sea squids of the families Cranchiidae, Gonatidae, and 10°C–25°C (Hunter & Macewicz 1985, Fitzhugh & Hettler
Bathyteuthidae (Laptikhovsky et al. 2007, 2019, Bush et al. 1995, Sauer et al. 2002, Macchi & Pájaro 2003, Macewicz et al.
2012). To date, POF have never been found in the ovaries of 2004, Melo & Sauer 2007, Whittames 2003). Thus, if the claim
immature Dosidicus, or in the ovary of any other immature of finding resting Dosidicus female were correct, the POF of
oegopsid or myopsid squids (e.g., Sauer & Lipinski 1990); POF these individuals would have been produced at maximum 2 days
appear only after mature oocytes have begun to ovulate and before collection, which seems an unrealistic time for a gonad to
they are always present in the gonad during the spawning cycle. enter the ‘‘resting’’ phase.
The first claim of postspawning ovary regeneration in In this study
s opinion, the ‘‘resting females’’ that described
Dosidicus gigas (Hernández-Muñoz et al. 2016) was difficult to in their study were normal immature females, with the ovary
challenge because the articles did not provide evidence of the showing regulatory atresia of early oocytes—a phenomenon
finding. Photos of POF in the studies (Fig. 1 in Hernández- well known for cephalopods including immature nektonic
Muñoz et al. 2016) were from mature gonads where POF ap- squids (e.g., Melo & Sauer 1998, Laptikhovsky et al. 2007). If
pearance is normal, arising as the first mature oocyte ovulates these immature Dosidicus gigas were in fact truly ‘‘resting,’’
and passes into the oviducts. Also, no distinction was made there would be atretic yolk oocytes in the ovary (they survive
between squid and fish maturation patterns. It was stated that much longer than POF) and a few residual ripe eggs in the
the presence of POF in the squid ovary is ‘‘evidence of previous oviducts remaining after the last spawning event. As both were
spawning’’ like in most fish species (Hernández-Muñoz et al. not reported, it is assumed that they were not found.
2016), thus misinterpreting the article by Melo and Sauer (1999) Ommastrephid squids mature once in their lifetime, but
in which the presence of POF was proven to be an evidence of they do so at different sizes. Up to three size-at-maturity
diurnal pattern of mature oocyte ovulation and probably a di- groups for Dosidicus gigas have been distinguished by
urnal pattern of egg release in batches. Moreover, first POF Nigmatullin et al. (2001) based on the size distribution of
appear in squid ovaries as first eggs ovulate, well before the mature squids. In the fisheries of the Gulf of California and
spawning event. Peru, two of those groups occur; however, the size at maturity
For Hernández-Muñoz et al. (2016), ‘‘spawning’’ seems to is likely a continuum (Hoving et al. 2013, Arkhipkin et al.
mean an instantaneous release of a single egg batch, rather than 2015), which in combination with variable environmental
the process of realizing the spawning potential during the re- factors may result in discrete sizes of adult squids of different
productive period in multiple batches. The main conclusion of seasonal and/or spatial cohorts. This key feature of com-
Hernández-Muñoz et al. (2016) reads: ‘‘female jumbo squid do plexity in the D. gigas population structure has been under-
not die after a single reproductive event. the consistent pres- estimated by Pérez-Palafox et al. (2019), who erroneously
ence of postovulatory follicles and the presence of oocytes of confounded the concept of size-at-maturity groups with that
different sizes and development support the hypothesis that the of annual cohorts. Cohorts are temporally defined size groups,
jumbo squid is a multiple spawner with more than one spawning typically linked to the season in which they hatch or to their
event during its life cycle.’’ This conclusion is correct if it is foraging area. Both size-at-maturity groups have independent
assumed that a single egg batch release corresponds to a ‘‘single stocks
dynamics driven by environmental factors (Hoving
spawning event.’’ Continuous production of yolk oocytes has et al. 2013). If the same squid stocks would be maturing con-
been reported previously in many studies (Ochoa-B áez sequently at both sizes, as suggested by an iteroparous strat-
1982, Arkhipkin 1992, Nigmatullin et al. 2001, Markaida egy, small size maturing squids would be normally more
2001, Dı́az-Uribe et al. 2006, Nigmatullin & Markaida 2009), abundant or at least occur in similar numbers to the large-size
as female Dosidicus lay egg masses intermittently in various group because of mortality. This, however, does not happen in
batches (i.e., they are batch-spawners) before they die, and their the squid fishery, where almost no mature females were found
reproductive period is extended as in all ommastrephid squids below 60 cm ML in ‘‘cold’’ years, whereas squids of the large-
(Nigmatullin & Markaida 2009). size maturing group are absent during ‘‘warm’’ years
The evidence for iteroparity in the second article (Pérez- (Arkhipkin et al. 2015).
Palafox et al. 2019) was based on ovarian structures found in It is important to have scientific consensus on the re-
immature ovaries in the study and that were claimed to be POF productive strategy of Dosidicus gigas because this squid

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 ITEROPARITY OR SEMELPARITY IN THE JUMBO SQUID DOSIDICUS GIGAS 377

supports the largest cephalopod fishery on the planet. For concerning a different reproductive strategy than previously
management of the fishery, understanding the reproductive reported and published thus far would be confusing and could
strategy is crucial. Introducing scientifically unsupported claims potentially compromise proper management of the resource.

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