Ruthenica, 1994, 4(1): 79-82.

Reproductive strategies in the squids of the family (preliminary report)

Ch.M.NIGMATULLIN and V.V.LAPTIKHOVSKY Atlantic Research Institute of Fisheries and Oceanography, 5 Dm. Donskoy Str., Kaliningrad 236000 Russia

The data are presented and analyzed on mature egg size, potential and relative fecundity, coefficient of vitelline oocytes, and peculiarities of maturation of female reproductive system in 17 species of all eleven genera of the family Omma­ strephidae. Two main reproductive strategies are outlined: offshore (/Ilex type, four subtypes) and oceanic (Sthenoteufhis type, three subtypes) ones. The form er is characteristic of relatively primitive subfamilies, the latter - of more evolutionarily advanced ones; some evolutionary vectors are observed in both strategies. Enhanced K-strategy is peculiar in the shelf-slope species and pronounced r-strategy - in the oceanic ones. There are considerable differences between adult females of the 1st and 2nd types in potential fecundity (in the 1 st type it is 5-10 times lower than in the 2nd) and relative fecundity (3-7 times) as weil as in the relative daily weight growth rates, but the reproductive investment (egg weight relative to female's body weight increase from the beginning of vitellogenesis up to early spawning state) is similar in both types, about 50-60%. The increase in fecundity during the penetration of a group into epipelagic biotopes of the open ocean is the general rule at least for squids and scombroid fishes.

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A number of mutually determined repro­ almost all ecologically important centers and ductive features of (reproductive stra­ climatic zones of the World Ocean, where they tegy), reflect in integral manner many pecu­ became dominating species. Their life cycles liarities of the ecosystem, the position of popu­ passes in different types of communities, thus lation in the biotic structure, and the influence of they are an appropriate object for the analysis of the controlling abiotic factors on the repro­ ecological implication of their reproductive stra­ duction. Nektonic ommastrephid squids pene­ tegies. There are only a few works on fecundity, trated in the process of adaptive radiation into egg size and peculiarities of spawning in several 80 Ch.M.Nigmatullin, V. V .Laptikhovsky species of the family [Petrov, 1977; Okutani, of ovary maturation in relation to duration of 1983; O'Dor, 1983; Harman et al., 1989; Nigma­ ontogenesis. tullin, Laptikhovsky, 1990; Laptikhovsky, Nig­ The following types of reproductive strategies matullin, 1992, 1993: Laptikhovsky, Zorikova, were revealed: 1992], but general patterns of reproductive stra­ tegies are still unknown. 1. Offshore strategy (type /Ilex). The matu­ The reproductive characteristics of female ration of the ovary is relatively long, gradual and squids were studied in 442 specimens belonging forestalls the maturation of the accessory glands. to 17 species of all 11 genera of this family. The ED is from 0.7-0.9 to 2.2 mm, in most species methods of study have been described earlier 0.9-1.2 mm; the egg weight 0.4-0.65 mg. PF [Nigmatullin et al., 1981; Nigmatullin, Lapti­ increases with body size growth; it is in different khovsky, 1990; Laptikhovsky, Nigmatullin, 1992, species 0.05-1.2 million eggs. RF in all species is 1993]. AJI species are monocyclic with asyn­ about 500-1500 egg/ g, except /. coindeti whose chronous oocyte development [Takahasi, Yaha­ RF may attain 2500 egg/g including the smallest ta, 1973; Burukovsky et al., 1977], their life eggs. CVO is 25-60% and decreases in species duration usually does not exceed one year except having !arge ripe eggs. Spawning lasts about in Martialia hyadesi and !arge individuals (mant­ 1-1.5 months (!Ilex), it is intermittent and with le length more than 70-80 cm) of Dosidicus gigas decreasing intensivity: after the end of the first and Ommastrephes bartramii [Arkhipkin,1989; period of egg accumulation in oviducts, the first A.I.Arkhipkin and A.B.Mikheev, pers. comm. ]. egg mass or several egg masses are laid (these All have a planktonic rhynchoteuthion larva with comprise 30-50% of actual fecundity); next mas­ mortality at this stage more than 95% [Okutani, ses comprise 15-5% (in I.argentinus the actual Watanabe, 1983; Laptikhovsky et al., 1993]. fecundity is about 70% of PF). During spawning Specimens of !Ilex argentinus, Todarodes an­ time the feeding activity initially declines, then golensis, D. gigas and two species of Stheno­ ceases, the body weight decreases up to 30-40% teuthis consitute the bulk (more than 80%) of the of the prespawning weight. Spawning occurs materials and were used as model species. Lite­ usually in offshore side of western and eastern rature data on Todarodes pacificus [Okutani, boundary currents, near the bottom of the shelf 1983] and partially Jllex illecebrosus [O'Dor, and continental slope; in several populations also 1983] were also used. Most of our conclusions are in the vicinity of oceanic islands and underwater based on the data on these species. In the model mountains. This strategy is typical for slope-shelf species, the animals at 1-6 (J.argentinus - 1-7) and neritic-oceanic species of Illicinae, Todarop­ maturity stages according to Nigmatullin's scale sinae and Todarodinae. [ 1989] have been studied. To study the rep­ 1.1 Illex spp., Todarodes pacificus. ED - roductive strategy pattern, we used: 0.7-0.9 mm, PF - 0.05-0.8 million eggs. 1. Ripe egg diameter (ED); to randomize the selection of the diameter measurements, the 1.2 Illex argentinus (slope-oceanic winter spa­ micrometer was placed in a horizontal position in wning group), Todarodes angolensis, ·T.filippo­ the eyepiece and the diameter parallel to gra­ vae, T.sagittatus (populations living off North­ duation of the micrometer was .measured in 50 West Africa, in the Cape Blanc region), Noto­ eggs). todarus spp., Todaropsis eblanae - ED - 1-1.3 2. Potential fecundity (PF); it was calculated mm, PF - 0.04-1.2 million eggs. as a sum of total oocyte number in the gonad and 1.3 Martialia hyadesi. ED - 1.55 mm, PF - egg number in both oviducts; this stock remains 0.25-0.6 million eggs. constant since immaturity (end of 2nd maturity stage) and up to the beginning of egg release 1.4 Todarodes sagittatus (populations inha­ during spawning; the actual fecundity is 60-80% biting the North Atlantic and the Mediterra­ PF, other oocytes are resorbed in spent females nean). ED - 2.2-2.4 mm, PF is more than 2 [Nigmatullin, Laptikhovsky, 1990; Laptikhovs­ million eggs; type of spawning may be specific ky, Nigmatullin, 1992, 1993; Laptikhovsky, Zori­ with declined share of potential fecundity that kova, 1992]. have being spawned. 3. Relative fecundity (RF); it is the ratio of PF to body weight in adult squids. 2. Oceanic strategy ( type). 4. Coefficient of vitelline oocytes (CVO); it is Ovary maturation occurs avalanche-Iike, rather the ratio of sum of the vitelline oocytes in gonad rapidly and lags behind maturation of the acces­ and ripe eggs in oviducts to PF in prespawning sory gland. ED - 0.7-1 mm, in most species - females; it shows the share of oocytes simul­ 0.75-0.85 mm, egg weight 0.2-0.24 mg. PF in­ taneously drawn into vitellogenesis and, there­ creases with the body size growth and in different fore, reflects the peculiarities of the yolk oocytes species varies from 0.1 to 22 million eggs, RF is stock replenishment and of the spawning. 2000-7000 egg/g, CVO is about 3-15%, mainly 5. Peculiarities of maturation of reproductive less than 10%. Spawning lasts for several months system, particularly the correlation between growth (Sthenoteuthis); it is intermittent and multi­ rates of ovary and accessory glands, the duration portional, with relatively stable intensity (egg Reproductive strategies in Ommastrephidae 81 numbers in the first and following egg masses are of PF, CVO, the peculiarities of the spawning comparable). Du ring spawning, active feeding is biotope) intermediate between type 1 and ocea­ maintained and significant somatic growth oc­ nic pelagic ommastrephids such as Stheno­ curs. Spawning is not connected with the bottom teuthis. All these features require the change of (the only exception are large-sized slope intra­ spawning type and mode of life with a tran­ specific groups of both species of Ornithoteuthis) sition to more expressed r-strategy and with a and occurs in epipelagic zone, usually at offshore need of active feeding in the spawning period; (oceanic) side of western and eastern boundary the latter circumstance is caused by necessity currents (California, Peru, Falkland, Brazil, Ca­ of additional energetic sources for extra ge­ nary Currents) and in open waters. This strategy nerative production. was revealed in neritic-oceanic Ornithoteuthinae Strengthening of K-strategy features in the and Dosidicus, and in oceanic . shelf-slope species and r-strategy features in the oceanic species occurs within the r part of the r-K 2.1 CVO is usually more than 10%: Orni­ continuum of . Nevertheless in some thoteuthis spp. (PF 0.05-0.7 million eggs) and species of each type (]Ilex, Ornithoteuthis, Dosi­ Dosidicus gigas (PF 0.3-13 million eggs); RF is dicus and Sthenoteuthis) one can observe some 1500-3500 egg/g. simultaneous and far-reaching microevolutionary 2.2 CVO is usually less than 10% tendencies towards r-strategy (nanisation and shortening of the life cycle with early maturation 2.2. l Sthenoteuthis spp., Ommastrephes bart­ and increase of RF) as well as towards K-strategy ramii and probably Eucleoteuthis luminosa. PF (size increase with retention of one-year life cycle 0.4-22 million eggs, RF 3000-7000 egg/g, CVO owing to high growth rates at early ontogenetic less than 10%. stages, subsequently going out of the control of 2.2.2 Hyaloteuthis pelagica and Sthenoteuthis common predators; in some cases also the in­ oualaniensis dwarf form (withou t dorsal pho­ crease of the egg size). tophore). PF about 0.1 million eggs, RF 6000- There are great differences in PF (by a factor 7000 egg/g, CVO 3-5%. of 5-10) and RF (by a factor of 3-7) between adult females of the same size belonging to lst The significant differences between the squids and 2nd types of the reproductive strategies. of types 1 and 2 were revealed in the male What this means is that significant differences in reproductive strategies too [Nigmatullin, Sabi­ reproductive effort are probable. Nevertheless, rov, 1987]. following the different relative daily weight The first type of reproductive strategies is growth rates in mature females, (about 0.5-1.0% characteristic of relatively primitive subfamilies, per day in l.argentinus [Arkhipkin, 1990] and the second one - for more evolutionarily ad­ 1.8-2.5% per day in S.pteropus [Arkhipkin, Mik­ vanced. The transition from the first to the heev, 1992]), we can estimate the "reproductive second type corresponds to the main direction of investment" expressed as total weight of eggs evolution of the family: the environmental alte­ produced by a female in relation to its body ration from initial slope-shelf biotopes to oceanic weight increase from beginning of the vitello­ epipelagic ones [Nigmatullin, 1979]. Ancestral genesis up to the full maturity or to early reproductive features mostly correspond to the spawning stage. In representatives of two alter­ group 1.1. Futhermore within each type of repro­ native reproductive strategies these values turned ductive strategy, the rows 1.1 - 1.2 - 1.3 and out to be similar: about 50-60%. This probably 1.4 on the one hand, and 1.1 - 2.1 - 2.2.1 and reflects the similarity in reproductive efforts in 2.2.2 on other hand appear to be the evolutionary both strategies. This fact corresponds to the vectors from primitive to more advanced forms. hypothesis that the reproductive effort does not Evolution of ommastrephids in the shelf and depend on the reproductive strategy but has an slope ecosystems and, further, in areas of under­ evolutionarily stable value [review: Kasyanov, water mountain occurrence (the row 1.1 - 1.2 - 1989]. 1.3 - 1.4), where predictability of the ecosystem We suppose that the increase in fecundity variability is relatively high, has a tendency during the p@netration of a group into the bio­ towards K-strategy (increase in the egg size with topes of epipelagic layers of the open ocean is the the retention of moderate level of fecundity). general rule at least for squids and scombroid During the penetration into oceanic pelagic wa­ fishes [Alexeev, Alexeeva, 1981 ]. However, in ters ( 1.1 - 2.1 - 2.2.1 and 2.2.2) with low squids this process shows itself more clearly due predictability of environmental variations causing to the necessity to spawn all reserve of ontogenic strong increase in the mortality, the increase in fecundity in a single reproductive season in PF occurred with the retention of initial egg size contrast to polycyclic fishes. that is minimal possible for cephalopods. Orni­ We sincerely thanks E.l.Alexeeva, A.l.Ar­ thoteutnis and Dosidicus occupied the most ocea­ khipkin, R.N.Burukovsky, K.N.Nesis, R.M.Sa­ nic "position" among neritic-oceanic forms and, birov and, especially, F. E.Alexeev for the fruitful therefore, are characterized by features (values discussion of results. 82 Ch.M.Nigmatullin, V. V .Laptikhovsky

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