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ITEROPARITY OR SEMELPARITY IN THE JUMBO SQUID DOSIDICUS GIGAS: A CRITICAL CHOICE.

Recently, two articles on the reproductive biology of the large nektonic jumbo squid Dosidicus gigas (d'Orbigny, 1835) (Ommastrephidae) have been published: Hernandez-Munoz et al. (2016) and Perez-Palafox et al. (2019). Both studies present a nearly identical claim of finding postovulatory follicles (POF) in immature females of D. gigas. Based on their findings, it was stated that D. gigas should be considered as iteroparous and that the ovary of this squid is subject to several cycles of maturation, spawning, and consequent recovery, with the gonad returning to the immature stage after each spawning phase.

If so, to our knowledge this would be a first case of iteroparity in oegopsid squids. Here, reasons why this claim is unfounded are discussed.

Currently, there is some uncertainty in the definitions used when describing reproductive strategies in cephalopods. This is largely due to the fact that there are two kinds of interpretation of parity in reproductive strategies. One considers the number of reproductive cycles or breeding opportunities in the life history, and the other considers the number of spawning activity events (i.e., repeatability of egg release) during each reproductive cycle or spawning season (Murua & Saborido-Rey 2003). Lamont Cole, who introduced the terms "semelparous" and "iteroparous," wrote: "... Some organisms are semelparous, that is to say, they reproduce only once in a lifetime.... iteroparous forms,... those which reproduce more than once in a lifetime..." (Cole 1954, p. 105), thus not stating anything about the repeatability of spawning events. The modern consensus, however, is that the terms monocyclic reproduction and semelparous are synonyms, as is the case for the terms polycyclic reproduction and iteroparous (Murua & Saborido-Rey 2003). For example, in fish: "in some species such a [gonad] cycle occurs only once before death; these are monocyclic or semelparous species (sensu Cole 1954) such as Anguilla or Oncorhynchus. In other species (polycyclic or iteroparous) this cycle occurs repeatedly every few years or every year" (Kamler 1992). Cephalopods generally do not live for many years, and in their case, the "semelparous species" simply implies that each animal during ontogenesis has only one reproductive cycle, and after the single spawning period, they die (Rocha et al. 2001).

The ovary of adult "iteroparous species" of cephalopods, after the first complete reproductive cycle, is then subjected to several sequential reproductive cycles, and the reproductive system reverts to the immature condition after each spawning period (Nigmatullin 2002, 2015). This condition was found in Vampyroteuthis infernales (Hoving et al. 2015) and its possibility has been suggested for Kondakovia longimana (Laptikhovsky et al. 2013).

An alternative point of view was expressed by Rocha et al. (2001) who criticized the semelparity-iteroparity concept because of the wide array of reproductive strategies found in cephalopods. Rocha et al. (2001) differentiated strategies between spawning once based on the ovary monocyclicity and spawning more than once based on either monocyclicity (most cephalopods) or polycyclicity (Nautilus).

Following the aforementioned interpretations of iteroparity and semelparity in cephalopods, the main conclusion of the studies by Hernandez-Munoz et al. (2016) and Perez-Palafox et al. (2019) is challenged, which, based on the presence of a resting gonadal phase, described Dosidicus gigas as a polycyclicity/iteroparous species.

Histological and morphological examination of oogenesis has been performed for several genera of ommastrephid squids, including Illex (Laptikhovsky & Nigmatullin 1992, Lin et al. 2017), Sthenoteuthis (Burukovsky et al. 1977, Laptikhovsky & Nigmatullin 2005), Todarodes (Hamabe 1963, Nigmatullin & Laptikhovsky 1994), Ornithoteuthis (Arkhipkin et al. 1998), and Dosidicus gigas (Ochoa-Baez 1982, Arkhipkin 1992, Markaida 2001, Diaz-Uribe et al. 2006, Nigmatullin & Markaida 2009). The overall conclusion of these studies was that ommastrephids do not exhibit ovarian polycyclicity. Once the ommastrephid gonad has reached the mature condition and produces ripe eggs, it never returns to the immature condition but continues to produce yolk oocytes until the ovary is spent and enters into a regressing phase. During this single period of ovary maturation, the reproductive system itself might be subjected to cycles of spawning events expressed in periodical replenishing and emptying of the oviducts during the production of pelagic egg masses. This spawning cyclicity may happen in squids with intermittent or continuous spawning because of asynchronous maturation of individual oocytes resulting in spawning of the eggs in different batches. In squids with synchronous oocyte maturation, the oviducts are filled and emptied just once in the life cycle. Examples of the latter include deep-sea squids of the families Cranchiidae, Gonatidae, and Bathyteuthidae (Laptikhovsky et al. 2007, 2019, Bush et al. 2012). To date, POF have never been found in the ovaries of immature Dosidicus, or in the ovary of any other immature oegopsid or myopsid squids (e.g., Sauer & Lipinski 1990); POF appear only after mature oocytes have begun to ovulate and they are always present in the gonad during the spawning cycle.

The first claim of postspawning ovary regeneration in Dosidicus gigas (Hernandez-Munoz et al. 2016) was difficult to challenge because the articles did not provide evidence of the finding. Photos of POF in the studies (Fig. 1 in Hernandez-Munoz et al. 2016) were from mature gonads where POF appearance is normal, arising as the first mature oocyte ovulates and passes into the oviducts. Also, no distinction was made between squid and fish maturation patterns. It was stated that the presence of POF in the squid ovary is "evidence of previous spawning" like in most fish species (Hernandez-Munoz et al. 2016), thus misinterpreting the article by Melo and Sauer (1999) in which the presence of POF was proven to be an evidence of diurnal pattern of mature oocyte ovulation and probably a diurnal pattern of egg release in batches. Moreover, first POF appear in squid ovaries as first eggs ovulate, well before the spawning event.

For Hernandez-Munoz et al. (2016), "spawning" seems to mean an instantaneous release of a single egg batch, rather than the process of realizing the spawning potential during the reproductive period in multiple batches. The main conclusion of Hernandez-Munoz et al. (2016) reads: "female jumbo squid do not die after a single reproductive event... the consistent presence of postovulatory follicles and the presence of oocytes of different sizes and development support the hypothesis that the jumbo squid is a multiple spawner with more than one spawning event during its life cycle." This conclusion is correct if it is assumed that a single egg batch release corresponds to a "single spawning event." Continuous production of yolk oocytes has been reported previously in many studies (Ochoa-Baez 1982, Arkhipkin 1992, Nigmatullin et al. 2001, Markaida 2001, Diaz-Uribe et al. 2006, Nigmatullin & Markaida 2009), as female Dosidicus lay egg masses intermittently in various batches (i.e., they are batch-spawners) before they die, and their reproductive period is extended as in all ommastrephid squids (Nigmatullin & Markaida 2009).

The evidence for iteroparity in the second article (Perez-Palafox et al. 2019) was based on ovarian structures found in immature ovaries in the study and that were claimed to be POF (Fig. 6 a-d in Perez-Palafox et al. 2019); however, their "POF" were actually sections of blood vessels (see Figure 1 in Lum Kong 1993) with attached primary oocytes subjected to atresia (see Figure 3b in Melo & Sauer 1998). In the figure caption, it was stated that "The postovulatory follicles are formed by fcs [follicular cells] supported by connective tissue constituted by reticular or collagenous elastic fibers when dyed blue, indicating that they are collagen fibers." This, in fact, is a description that perfectly fits a typical composition of animal blood vessels, including those of squids (Shadwick 1999). The "POF" described in Perez-Palafox et al. (2019) look rather different from "real" POF, as described in Hernandez-Munoz et al. (2016) Figure 1, panel 8, and which were well described for Loligo reynaudii (Melo & Sauer 2007).

The degeneration of POF takes less than 48 h (often less than 24 h) in subtropical and temperate squids and fish spawning at 10[degrees]C-25[degrees]C (Hunter & Macewicz 1985, Fitzhugh & Hettler 1995, Sauer et al. 2002, Macchi & Pajaro 2003, Macewicz et al. 2004, Melo & Sauer 2007, Whittames 2003). Thus, if the claim of finding resting Dosidicus female were correct, the POF of these individuals would have been produced at maximum 2 days before collection, which seems an unrealistic time for a gonad to enter the "resting" phase.

In this study's opinion, the "resting females" that described in their study were normal immature females, with the ovary showing regulatory atresia of early oocytes--a phenomenon well known for cephalopods including immature nektonic squids (e.g., Melo & Sauer 1998, Laptikhovsky et al. 2007). If these immature Dosidicus gigas were in fact truly "resting," there would be atretic yolk oocytes in the ovary (they survive much longer than POF) and a few residual ripe eggs in the oviducts remaining after the last spawning event. As both were not reported, it is assumed that they were not found.

Ommastrephid squids mature once in their lifetime, but they do so at different sizes. Up to three size-at-maturity groups for Dosidicus gigas have been distinguished by Nigmatullin et al. (2001) based on the size distribution of mature squids. In the fisheries of the Gulf of California and Peru, two of those groups occur; however, the size at maturity is likely a continuum (Hoving et al. 2013, Arkhipkin et al. 2015), which in combination with variable environmental factors may result in discrete sizes of adult squids of different seasonal and/or spatial cohorts. This key feature of complexity in the D. gigas population structure has been underestimated by Perez-Palafox et al. (2019), who erroneously confounded the concept of size-at-maturity groups with that of annual cohorts. Cohorts are temporally defined size groups, typically linked to the season in which they hatch or to their foraging area. Both size-at-maturity groups have independent stocks' dynamics driven by environmental factors (Hoving et al. 2013). If the same squid stocks would be maturing consequently at both sizes, as suggested by an iteroparous strategy, small size maturing squids would be normally more abundant or at least occur in similar numbers to the large-size group because of mortality. This, however, does not happen in the squid fishery, where almost no mature females were found below 60 cm ML in "cold" years, whereas squids of the largesize maturing group are absent during "warm" years (Arkhipkin et al. 2015).

It is important to have scientific consensus on the reproductive strategy of Dosidicus gigas because this squid supports the largest cephalopod fishery on the planet. For management of the fishery, understanding the reproductive strategy is crucial. Introducing scientifically unsupported claims concerning a different reproductive strategy than previously reported and published thus far would be confusing and could potentially compromise proper management of the resource.

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VLADIMIR LAPTIKHOVSKY, (1*) ALEXANDER ARKHIPKIN, (2) MAREK R. LIPIINISKI, (3) UNAI MARKAIDA, (4) HILARIO MURUA, (5) CHINGIZ M. NIGMATULLIN, (6) WARWICK H. H. SAUER (3) AND HENK-JAN T. HOVING (7)

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

(*) Corresponding author. E-mail: vladimir.laptikhovsky@cefas.co.uk

DOI: 10.2983/035.038.0218
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Author:Laptikhovsky, Vladimir; Arkhipkin, Alexander; Lipiiniski, Marek R.; Markaida, Unai; Murua, Hilario;
Publication:Journal of Shellfish Research
Article Type:Report
Geographic Code:4EUUK
Date:Aug 1, 2019
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