A review of reproductive strategies in cephalopods

Biol. Rev. (2001), 76, pp. 291–304 Printed in the United Kingdom " Cambridge Philosophical Society 291

A review of reproductive strategies in

cephalopods

FRANCISCO ROCHA*, A; NGEL GUERRA and A; NGEL F. GONZA; LEZ

Instituto de Investigaciones Marinas (CSIC), C}Eduardo Cabello 6, 36208 Vigo, Spain

(Received 25 September 2000; revised 29 January 2001; accepted 29 January 2001)

ABSTRACT

Cephalopod reproductive strategies are reviewed in order to clarify their current, confusing status. Based onthe type of ovulation, spawning pattern and growth between egg batches or spawning periods, fivecomprehensive and flexible cephalopod reproductive strategies are defined. Accordingly, with these threefactors the following classification is proposed. (a) Spawning once (formerly semelparity) consisting ofsimultaneous terminal spawning, with synchronous ovulation, monocyclic spawning and absence of growthbetween egg batches. (b) Spawning more than once (formerly iteroparity) including: (i) polycyclic spawningwith egg-laying occurring in separate batches during the spawning season and growth occurring betweenproduction of egg batches and spawning seasons ; (ii) multiple spawning, with group-synchronous ovulation,monocyclic spawning and growth between egg batches ; (iii) intermittent terminal spawning, with group-synchronous ovulation, monocyclic spawning and no growth between egg batches ; (iv) continuousspawning, with asynchronous ovulation, monocyclic spawning and growth between egg batches. Examplesof species exhibiting each of these reproductive strategies are given. The large amount of inter-speciesvariation in several life-history traits related to reproductive events is discussed.

Key words : Cephalopoda, reproduction, reproductive strategies, spawning patterns, behaviour, ecology.

CONTENTS

I. Introduction ............................................................................................................................ 292II. The ovulation and spawning pattern approach ...................................................................... 293

(1) Ovulation pattern ............................................................................................................. 293(2) Spawning pattern.............................................................................................................. 293

III. Some examples of reproductive strategies in coleoid cephalopods........................................... 293(1) Sepiida Keferstein, 1866.................................................................................................... 293(2) Sepiolida Grimpe, 1921..................................................................................................... 294(3) Idiosepiida Grimpe, 1921.................................................................................................. 294(4) Teuthida Naef, 1916 ......................................................................................................... 295(5) Cirroctopoda Young, 1989................................................................................................ 295(6) Octopoda Leach, 1818...................................................................................................... 295

IV. Characterisation of the reproductive pattern in cephalopods.................................................. 296(1) Spawning once (formerly semelparity) ............................................................................. 296

(a) Simultaneous terminal spawning ................................................................................ 296(2) Spawning more than once (formerly iteroparity) ............................................................. 296

(a) Polycyclic spawning .................................................................................................... 296(b) Multiple spawning ...................................................................................................... 296(c) Intermittent terminal spawning.................................................................................. 296(d) Continuous spawning.................................................................................................. 298

* Corresponding author. E-mail : frocha!iim.csic.es

292 Francisco Rocha, A; ngel Guerra and A; ngel F. Gonza! lez

V. An alternative ‘ecological ’ classification.................................................................................. 298VI. Reproductive strategies as adaptations to ecosystem demands................................................ 299

VII. Conclusions .............................................................................................................................. 300VIII. Acknowledgements .................................................................................................................. 301

IX. References................................................................................................................................ 301

I. INTRODUCTION

The production of viable offspring by sexualorganisms is the outcome of both sexual and naturalselection, the actions of which may be antagonistic(Bell, 1997), but both of which follow the sameprinciples (Hanlon & Messenger, 1996). Maximumreproductive output is reached through a so-calledreproductive strategy, i.e. a ‘complex adaptation’(Stearns, 1992), favoured by selection and encodedin the genome of each species. The reproductivestrategy of any species consists of a broad spectrum oftactics that enable individuals to achieve theirreproductive goal.

Given the very different life-styles and body formsof cephalopods resulting from ecological and demo-graphic pressures during past evolutionary processes,one should expect their reproductive strategies to bequite variable.

Any reproductive strategy may subsume differenttactics that might be classified in groups. Thus,Hanlon & Messenger (1996) consider : (i) intrasexualselection (e.g. male fighting tactics) and (ii) in-tersexual selection (e.g. female choice and maleornamentation) as tactics favoured by sexual selec-tion, along with; (iii) mating system (e.g. spermcompetition); and (iv) spawning pattern (e.g.semelparity and iteroparity). We focus our review ofthe reproductive strategies in cephalopods on thelast-mentioned of these groups of tactics, namelyspawning patterns.

Until recently, practically all living cephalopodswere considered to be semelparous marine molluscsthat lay their eggs in one single spawning, afterwhich they would die (Boyle, 1983; Calow, 1987;Rodhouse, 1998). The only exception to this patternwas supposed to be Nautilus, with species having alife-span longer than 20 years. Nautilus species shouldbe considered as iteroparous because the femalesspawn once a year, survive, feed, grow and re-generate their gonads for a further reproductiveevent the following year (Ward, 1987). However,Boletzky (1981, 1986), Rodaniche (1984), Mangold(1987), Harman et al. (1989), and Mangold, Young& Nixon (1993) have cautioned that more variation

exists in the reproductive traits of coleoidcephalopods than was previously realised.

Based on these variations, several reproductivestrategies have been defined for cephalopods withregard to the oocyte maturation process and the typeof spawning in each species (Boletzky, 1981, 1986;Harman et al., 1989; Villanueva, 1992; Mangold et

al., 1993; Gonza! lez, 1994; Rocha, 1994; Boyle,Pierce & Hastie, 1995; Nesis, 1996; Rasero, 1996;Rocha et al., 1996; Rocha & Guerra, 1996;Nigmatullin & Laptikhovsky, 1994, 1999). However,the current definitions for different cephalopodreproductive strategies are, in general, confusing.Among the most important reasons for the confusionis the ambiguity in the use of the terms ‘ iteroparity ’and ‘semelparity ’. Moreover, the maturation pro-cess of the oocytes in the ovary is practicallyunknown for many species of cephalopods.

Cephalopod life-cycles are somewhat enigmatic(Calow, 1987). Boletzky (1981) attributes some ofthe enigmas of their life-cycles (e.g. the apparentubiquity of breeding once and post-reproductivemortality of the parents) to a combination of r- andK-factors and presumably r- and K-selection (sensuMacArthur & Wilson, 1967) operating in onespecies. However, it is probably more appropriate todepict life-cycles as complex sets of covarying traits,some combinations of which might involve so-calledr-, others K-, and yet others a combination of r- andK-traits (Sibly & Calow, 1985). Ultimately in-formation on reproductive strategies in cephalopodsmay lead to a better understanding of the evolutionof cephalopod life-histories.

In this paper, therefore, we review the existinginformation on this subject and attempt to definepatterns in cephalopod reproductive strategies.These definitions are based on the type of ovulation,the spawning pattern and whether or not somaticgrowth between egg batches occurs. Examples ofspecies exhibiting any of the defined reproductivestrategies are also given. The large amount of inter-species variation in certain life-history traits relatedto reproductive events is demonstrated and dis-cussed.

293A review of reproductive strategies in cephalopods

II. THE OVULATION AND SPAWNING

PATTERN APPROACH

(1) Ovulation pattern

Ovaries may be distinguished as synchronous, group-synchronous and asynchronous ovulation accordingto oocyte formation and development. FollowingMarza (1938, in Wallace & Selman, 1981), in asynchronous ovary ‘all oocytes, once formed, growand ovulate from the ovary in unison, furtherreplenishment of one stage by an earlier stage doesnot take place’. Such ovaries may be found in teleostfishes, which spawn once and then die, such as someanadromous salmon species and catadromous eels.In a group-synchronous ovary, ‘at least two popu-lations of oocytes can be distinguished at some time;a fairly synchronous population of large oocytes(defined as a ‘‘clutch’’) and a more heterogeneouspopulation of smaller oocytes from which the clutchis recruited. This is by far the most common situationamong teleosts ’ (Wallace & Selman, 1981). In anasynchronous ovary, ‘oocytes of all stages are presentwithout dominant populations ’ (Wallace & Selman,1981). This situation appears to apply to someteleost species (e.g. Fundulus heteroclitus Linnaeus,1758). Although Wallace & Selman (1981) ac-knowledge that placing labels on life-history patternsis a simplification and that such patterns probablyexist along a continuum, distinction of differentnodes along the continuous aids the understandingof life-history patterns.

(2) Spawning pattern

Before we start to discuss the meaning of iteroparity,the definition of this term should be mentioned.Thus, following the Oxford Dictionary of Zoology,iteroparity has been defined as ‘ the condition of anorganism that has more than one reproductive cycleduring its lifetime’. In other words, iteroparousanimals are those that return, after every spawningevent, to the preparatory phase through a re-productive resting phase. In that sense, Nautilus isthe only iteroparous cephalopod.

Stearns’ (1992) view of the evolution of life-historypatterns follows Cole’s (1954) original definition thatiteroparous organisms have more than one repro-ductive event in their lifetime whereas semelparousorganisms reproduce only once. Considering theoriginal definition, which is not dependent onmultiple seasons (supposing regression of ovaries), acephalopod will be iteroparous if it spawns morethan once and semelparous if it spawns only once.

However, many cephalopod species, namely thesepioids, many teuthids, the epipelagic incirrateoctopods and the cirrates spawn repeatedly in onespawning season, which could produce confusionwhen identifying iteroparous or semelparouspatterns. In such cases, it will be necessary todistinguish if the egg capsules are released sim-ultaneously (semelparous) or with a significant timeinterval between successive eggs spawned one by oneor successive egg batches (iteroparous).

Boletzky (1987) indicated the possible existence ofiteroparity in cephalopods. However, many cepha-lopod workers seem reluctant to use the worditeroparity. For example, Harman et al. (1989),Mangold et al. (1993) and Rocha et al. (1996) do notclassify as iteroparous such cephalopods as theommastrephid squid Sthenoteuthis oualaniensis (Lesson,1830), which matures additional oocytes and growsbetween reproductive bouts. In that respect,Mangold (1987) stated: ‘ so far, the only cephalopodknown to breed in several seasons (years), commonlyreferred to as iteroparous, is Nautilus ’. Moreover,some authors (e.g. Moltschaniwskyj, 1995) havesuggested that iteroparity is not possible for mostcephalopods because they have life-spans of one yearor less. However, there is no reason to attach a fixedlength of time to the definition of iteroparity.Although semelparous organisms are generallythought to have short life-spans, some may live for40–60 years (Stearns, 1992; Young, 1990) and stillare classified as semelparous. However, iteroparousorganisms are generally thought to have longer life-spans. Also, if animals must reproduce in more thanone season to be considered iteroparous, those thathave short life-spans are automatically eliminatedregardless of their reproductive pattern.

III. SOME EXAMPLES OF REPRODUCTIVE

STRATEGIES IN COLEOID CEPHALOPODS

Some examples of reproductive strategies withincephalopods are mentioned here in order to illustratethe existing confusion. The classification of therecent Cephalopoda proposed by Boletzky (1999) isused in this paper.

(1) Sepiida Keferstein, 1866

Females of the common cuttlefish Sepia officinalis

Linnaeus, 1758 are known to spawn intermittentlyover a period of up to 4 months in captivity(Boletzky, 1987). One individual female of this


species maintained under aquarium conditions,however, showed intermittent spawning of ninebatches of eggs over 7 months. During this period thefemale mated twice but its body size did not increasebetween spawning events (Boletzky, 1988). As statedby Boletzky (1988): ‘ the fact that the physiology ofthe animal allows long-continued spawning does notprove that this capacity is always fully exploitedunder natural conditions ; it only proves that thepossibility of such protracted spawning really exists,and it suggests that this possibility becomes im-portant under certain environmental conditions tocounterbalance high mortality rates ’.

(2) Sepiolida Grimpe, 1921

Gabel-Deickert (1995) showed that the sepiolidsSepiola affinis Naef, 1912; Sepiola rondeleti Leach, 1834;Sepiola intermedia Naef, 1912; Sepietta obscura Naef,1916, and a Sepietta sp. are intermittent spawners.

(3) Idiosepiida Grimpe, 1921

Idiosepius pygmaeus Steenstrup, 1881, a very smallcuttlefish, was identified as iteroparous. Lewis &Choat (1993) stated: ‘ this species is functionallyiteroparous from both an endocrine and physio-logical perspective’. They presented evidence thatreproduction and growth occurs simultaneously inmature animals. I. pygmaeus fed ad libitum incor-porates 5±1 times its body mass into reproductivematerial while less well-fed animals put 2±8 timestheir body mass into reproduction (Lewis & Choat,1993). It is interesting to note that this species hasone of the shortest life-spans and smallest adult sizesof cephalopods. Jackson (1989) reported that it livesfor 80 days or less, and Nesis (1996) indicated that I.pygmaeus lays egg batches during most of its adult life.

(4) Teuthida Naef, 1916

The loliginid squid Loligo opalescens Berry, 1911, andthe ommastrephid squid Todarodes pacificus pacificus

(Steenstrup, 1880) have a type of reproductivestrategy where ovulation is synchronous, egg-layingoccurs in a very short period at the end of theanimal’s life, and there is no oocyte maturationduring the spawning period (Hixon, 1983; Ikeda,Sakurai & Shimazaki, 1993). This also occurs in themajority of the species of the family Gonatidae(Nesis, 1996). This type of reproductive pattern hasbeen named ‘terminal spawning’ (Hixon, 1983),‘ single spawning’ (Mangold et al., 1993) and

‘simultaneous terminal spawning’ (Rocha et al.,1996).

One example of iteroparity according to thedefinition proposed by Cole (1954) is observed withSthenoteuthis oualaniensis. Harman et al. (1989) statedthat : ‘after spawning once, S. oualaniensis apparentlycontinues to feed, grow, and mature additionaloocytes before spawning again’, although the gonadsdo not regress and subsequently redevelop. Sny$ der(1998) found a large proportion of maturing andpre-vitellogenic oocytes in the ovary of maturefemales of this species, which suggests that eggs arelaid periodically. However, in both papersmentioned above this reproductive strategy wasnamed ‘multiple spawning’. Harman et al. (1989)indicated that multiple spawning includes ‘all typesof non-semelparous reproduction’.

The diamond-shaped squid Thysanoteuthis rhombus

Troschel, 1857, was considered to be an intermittentspawner by Nigmatullin, Arkhipkin & Sabirov(1995). Asynchronous development of oocytes in theovary, with six size groups of oocytes, was found.Nigmatullin et al. (1995) indicated: ‘ it is possiblethat T. rhombus has multiple spawning of the‘‘pulsate ’’ type, i.e. with successive fillings andevacuations of the oviducts ’. Thus, during thespawning period, which lasts 2–3 months, a femaleT. rhombus may produce approximately 8–12 eggmasses if it utilises all of its vitelline oocytes(Nigmatullin et al., 1995).

According to Cole’s (1954) iteroparity definition,an undescribed tropical Photololigo species is alsoiteroparous (Moltschaniwskyj, 1995). Baeg, Sakurai& Shimazaki (1993) observed that egg developmentin ovaries of Loligo bleekeri Keferstein, 1866, is highlyasynchronous, which may indicate that this speciesspawns in batches during its spawning season.Segawa (1987) found a group-synchronous ovulationpattern in the loliginid squid Sepioteuthis lessoniana

Fe! russac, 1830, and Wada & Kobayashi (1995)reported that this species is iteroparous.

Recently, Sauer & Lipin! ski (1990) and Melo &Sauer (1999) provided histological evidence ofmultiple spawning by analysing the ovary matu-ration and the spawning pattern of the chokka squidLoligo vulgaris reynaudii Orbigny, 1839. Melo & Sauer(1998) found the presence of partially spent ovariescontaining post-ovulatory follicles alongside oocytesin various stages of vitellogenesis and the presence ofatretic oocytes in developing and spent ovaries.Furthermore, Sauer, Melo & Wet (1999) showedthat L. vulgaris reynaudii is capable of multiplespawning under laboratory conditions. A recent


study of Sauer, Lipin! ski & Augustin (2000) considersthis squid as a uniseasonal-iteroparous species thatdeposits distinct egg clutches over an extendedperiod in a number of spawning sites.

There are many examples of the so-called ‘ inter-mittent spawning pattern’ (Boletzky, 1975) or‘ intermittent terminal spawning pattern’ (Rocha et

al., 1996) in squids. Thus, the loliginid squids Loligo

vulgaris Lamarck, 1798, Loligo forbesi Steenstrup,1856, Loligo pealeii Lesueur, 1821, and Loligo gahi

Orbigny, 1835 (Rocha & Guerra, 1996; Collins,Burnell & Rodhouse, 1995; Maxwell, 1998; Hatfield& Murray, 1999), and the ommastrephid squids Illex

coindetii (Ve! rany, 1839), Todaropsis eblanae (Ball,1841) and Illex illecebrosus (Lesueur, 1821) (Gonza! lez& Guerra, 1996; Rasero, 1996; O’Dor & Dawe,1998) were included in this category. In thisreproductive pattern, oocyte maturation and egg-laying occur in separate batches during the spawningperiod, which is usually relatively long, although inno case does it represent the greater part of theanimal’s life. However, in these species, contrary towhat occurs in Sthenoteuthis oualaniensis (Harman et

al., 1989), it seems that somatic growth does not takeplace between spawning events. This is why theyshould not be classified as multiple spawners.However, according to Cole’s (1954) definition ofiteroparity these squids could be considered asiteroparous.

(5) Cirroctopoda Young, 1989

Deep-sea cirroctopods Opisthoteuthis agassizii Verril,1883; Opisthoteuthis vossi Sa! nchez & Guerra, 1989,and Opisthoteuthis californiana (Berry, 1949) have atype of reproductive strategy in which asynchronousovulation occurs with a continuous production ofova once spawning has commenced, so that adultsspawn many times during their extended life-spans,as in the cirrate octopod Grimpoteuthis glacialis

(Robson, 1930) (Villanueva, 1992; Laptikhovsky,1999; Vecchione, Piatkowski & Allcock, 1998). Thistype of reproductive strategy was named ‘continuousspawning’ (Villanueva, 1992). Aldred, Nixon &Young (1983) found that female Cirrothauma murrayi

Chun, 1911, had eggs of a large size range in theirovaries, and proposed that this species may con-tinuously lay eggs once mature. This strategy couldbe common among cirrate octopods, all of whichapparently lay large eggs protected by a hard coatproduced by the oviducal gland so the eggs do notneed to be brooded (Boletzky, 1982; Mangold,1987). According to Cole’s (1954) iteroparity

definition these species should be considered asiteroparous.

It should be noted that Opisthoteuthis vossi wasrecently considered a junior synonym of Opisthoteuthis

grimaldii (Joubin, 1903) (Boyle, Collins &Williamson, 1998; Villanueva, 2000), and Grim-poteuthis glacialis was transferred to the genus Cirroc-topus (O’Shea, 1999).

(6) Octopoda Leach, 1818

The octopod Octopus chierchiae Jatta, 1889, laid eggsfour times in the laboratory and grew betweenreproductive events (Rodaniche, 1984). This re-productive behaviour was interpreted as iteroparity.Boletzky (1987) stated: ‘whether to call this situationiteroparity or intermittent spawning is largely amatter of taste, unless we reserve the former term torepeated seasonal reproduction. What is importantat the population level is the tendency to break thelimitation in holding capacity of the gonad byprolonged ovary functioning with successive eggmaturation. ’ Further examples of iteroparity inOctopoda can be found in Argonauta boettgeri

Maltzan, 1881, and Argonauta hians Lightfoot, 1786(Nesis, 1977). Moreover, evidence exists for multiplespawning in deep-sea octopods. Thus, Kuehl (1988)found that Pareledone charcoti (Joubin, 1905) andPareledone polymorpha (Robson, 1930) had a widerange of sizes of maturing ova that could indicaterepeated spawning. Similar evidence was found inBenthoctopus piscatorum (Verrill, 1879) (Nixon, 1991).However, almost all octopods are clearly ‘ terminalspawners ’ (Nesis, 1996).

When discussing the terms multiple or inter-mittent spawning in deep-sea Octopodidae, it isnecessary to bear in mind that females of theseoctopuses brood egg batches during long periods,many months and probably several years, and dieafter hatching of paralarvae, as occurs in almost allknown Octopodidae (e.g. Voight & Grehan, 2000).Thus, they may lay eggs in their only clutch duringa more or less protracted period but definitely do notlay clutches repeatedly. Therefore, one may divideoctopodids into a group of small-egged species layingeggs in festoons and simultaneously (some species ofOctopus and Eledone) and large-egged ones layingeggs singly and probably capable of adding eggsduring a more or less extended period but alwaysbelonging to the same egg-clutch (some Octopus,Benthoctopus and Bathypolypus). Deep-sea octopodssuch as Pareledone charcoti, Pareledone polymorpha andBenthoctopus piscatorum have a group-synchronous


ovulation pattern (Kuehl, 1988; Nixon, 1991) thatwould suggest this type of reproductive strategy.These cases are clearly two ends of a continuum. Forexample, the whole egg-clutch of Enteroctopus dofleini

(Wu$ lker, 1910) (laying rather small eggs in festoons)may weigh approximately 2 kg; it is thereforeunlikely that all festoons are spawned in the samenight (K. N. Nesis, personal communication).

IV. CHARACTERISATION OF THE

REPRODUCTIVE PATTERN IN CEPHALOPODS

As highlighted in the previous discussion, it seemsthat the most outstanding problem is the confusioninvolving the terms iteroparity and semelparity indefinitions for cephalopod reproductive strategies.In order to avoid such difficulty, we propose toreplace the terms semelparity with ‘ spawning once’and iteroparity with ‘ spawning more than once’, inother words to refer exclusively to the spawningpattern (Kirkendall & Stenseth, 1985). Also, it isnecessary to consider in greater detail the dynamicaspects of oocyte growth in the ovary and howoocytes develop. In this regard, it is interesting todistinguish between ovaries with synchronous,group-synchronous and asynchronous ovulation(Wallace & Selman, 1981). Finally, the presence orabsence of somatic growth between production ofegg batches should be used as a third criterion toobtain a suitable classification of reproductivepatterns.

Taking these considerations into account, thefollowing classification for the known reproductivestrategies is proposed (Table 1).

(1) Spawning once (formerly semelparity)

(a) Simultaneous terminal spawning

This is a type of spawning where ovulation issynchronous, and there is no oocyte maturationduring the spawning period. The egg spawningpattern is monocyclic and the egg-laying occurs in avery short period at the end of the animal’s life. Todate, some of the species that have been found toexhibit simultaneous terminal spawning include:Loligo opalescens and Todarodes pacificus pacificus amongsquids (Hixon, 1983; Ikeda et al., 1993), and Octopus

cyanea Gray, 1849; Octopus vulgaris Cuvier, 1797;Octopus mimus Gould, 1852; Vitreledonella sp., andHaliphron sp. among octopods (Van Heukelem, 1983;Mangold et al., 1993; Cortez, Castro & Guerra,

1995; Nesis, 1996) (Table 1). The only differencebetween squid and octopod simultaneous terminalspawners is that the latter lay eggs in a den, whichare cared for the mother (most Octopodidae), orcarried by female arms (some species of Octopus andHapalochlaena, all Bolitaenidae, Alloposidae,Tremoctopodidae), or they are incubated in theoviducts (ovoviparity) up to hatching paralarvae(Vitreledonellidae, Ocythoidae) (Nesis, 1996)whereas squids do not show parental care of the eggs.

(2) Spawning more than once (formerlyiteroparity)

(a) Polycyclic spawning

This is a reproductive strategy where the spawningpattern shows several cycles and the gonads re-generate after each breeding period, making newreproductive cycles possible (Table 1). Thereappears to be a single spawning season each yearwith the animal surviving, feeding and growingbetween spawning events. Eggs mature in severaldistinct clutches and egg-laying occurs in separatebatches during each spawning period (Ward, 1983;Arnold, 1987). The species of the genus Nautilus havebeen found to exhibit polycyclic spawning (Ward,1983, 1987).

(b) Multiple spawning

In this pattern, group-synchronous ovulation occursin the ovary (Harman et al., 1989). The spawningpattern is monocyclic and egg-laying occurs inseparate batches, somatic growth continuing be-tween separate spawning events. To date, this typeof ovulation has been described in several species(Table 1), e.g. Octopus chierchiae, Sthenoteuthis

oualaniensis, Ommastrephes bartramii (Lesueur, 1821)and Dosidicus gigas (Orbigny, 1835) (Rodaniche,1984; Harman et al., 1989; Nigmatullin &Laptikhovsky, 1994; Nesis, 1970, 1996).

(c) Intermittent terminal spawning

In this type of spawning, group-synchronous ovu-lation occurs in the ovary. Spawning is monocyclicand egg-laying occurs in separate batches during thespawning period, which is usually relatively long,although in no case does it represent the greatestfraction of the animal ’s life. This type of strategydiffers from ‘multiple spawning’ in that somaticgrowth does not take place between spawning events.


Table 1. Classification of reproductive strategies in cephalopods, with some examples

Characteristics of thereproductive pattern

Growth betweenegg batches orspawning seasons

Name of thereproductivestrategy Representative species

Spawning once

Synchronous ovulation

1. Monocyclic spawning

Egg-laying occurssimultaneously

No Simultaneousterminalspawning

Loligo opalescens

Todarodes pacificus pacificus

Octopus mimus

Octopus vulgaris

Octopus cyanea

Vitreledonella sp.Haliphron sp.

Spawning more than once

Group-synchronous ovulation

1. Polycyclic spawning

Egg-laying occurs inseparate batches duringdifferent spawning seasons(ovary regeneration)

Yes Polycyclicspawning

Nautilus spp.


Egg-laying occurs inseparate batchesduring the samespawning (no ovaryregeneration)

Yes Multiplespawning

Sthenoteuthis oualaniensis

Dosidicus gigas

Ommastrephes bartramii

Hyaloteuthis pelagica

Octopus chierchiae


Egg-laying occurs inseparate batches

No Intermittentterminalspawning

Sepia officinalis

Sepioteuthis lessoniana

Photololigo sp.Loligo vulgaris

Loligo forbesi

Loligo pealei

Loligo bleekeri

Berryteuthis magister

Todaropsis eblanae

Todarodes angolensis

Illex coindetii

Illex argentinus

Martialia hyadesi

Asynchronous ovulation


Egg-laying occurs inan extended andcontinuous spawningperiod in relation tothe animal’s life

Yes Continuousspawning

Idiosepius pygmaeus

Cirrothauma murrayi

Opisthoteuthis agassizii

Opisthoteuthis californiana

Opisthoteuthis grimaldii

Grimpoteuthis glacialis

Bathypolypus arcticus

Benthoctopus piscatorum

Argonauta boettgeri

Argonauta hians


The species Sepia officinalis, Loligo vulgaris reynaudii,Loligo bleekeri, Loligo vulgaris vulgaris, Loligo forbesi,Illex coindetii, Todaropsis eblanae and Todarodes

angolensis (Boletzky, 1987, 1988; Melo & Sauer,1999; Baeg et al., 1993; Rocha & Guerra, 1996;Collins et al., 1995; Gonza! lez & Guerra, 1996;Rasero, Gonza! lez & Guerra, 1995; Nigmatullin &Laptikhovsky, 1999) should be considered inter-mittent terminal spawners (Table 1). Individualexceptions do exist, however; e.g. Sepia officinalis

where continuous spawning may occur. On theother hand, probably most of the deep-water squids,including Gonatidae, Ancistrocheiridae, Onycho-teuthidae, Cranchiidae, etc. are also intermittentterminal spawners (Jackson & Mladenov, 1994;Arkhipkin, 1997; Arkhipkin & Nigmatullin, 1997;Nesis, 1997; Nesis, Nigmatullin & Nikitina, 1998).This could be explained by the large eggs producedby these deep-water animals, causing the oviductvolume to be insufficient to accommodate all eggs.Therefore, the number of egg masses must bespawned in several batches (K. N. Nesis, personalcommunication).

(d) Continuous spawning

In this type of reproductive strategy, ovulation ischaracterised by continuous asynchronousproduction of ova in the ovary after spawning hascommenced (Villanueva, 1992). In this monocyclicspawning pattern, adults spawn continuously duringtheir relatively extended life-spans and somaticgrowth takes place during spawning events (Table1). This strategy is present in cirroctopods, includingCirrothauma murrayi, Opisthoteuthis agassizii, Opistho-teuthis grimaldii and Grimpoteuthis glacialis (Aldred et

al., 1983; Villanueva, 1992; Vecchione et al., 1998).The pelagic octopods Argonauta boettgeri andArgonauta hians seem to have a similar strategy (Nesis,1977, 1996). The dwarf squid Idiosepius pygmaeus canbe also considered a continuous spawner because,living for only 80 days (Jackson, 1989), it lays eggbatches continuously during most of its adult life(Lewis & Choat, 1993; Nesis, 1996).

V. AN ALTERNATIVE ‘ECOLOGICAL’

CLASSIFICATION

Some Russian teuthologists such as Nigmatullin &Laptikhovsky (1994, 1999), Nesis (1996) andLaptikhovsky (1998) defined alternative repro-ductive strategies for cephalopods that ‘reflect in an

integral manner many peculiarities of the ecosystem,the position of populations in the biotic structure,and the influence of the controlling abiotic factors onreproduction’ (Nigmatullin & Laptikhovsky, 1994).These reproductive strategies are independent ofearlier treatment by other authors. However, theycan easily be related to the reproductive patternsdescribed above. The two main strategies defined byNigmatullin & Laptikhovsky (1994), are an ‘off-shore strategy (Illex type) ’ and an ‘oceanic strategy(Sthenoteuthis type) ’. These strategies correspond toour intermittent terminal spawning and multiplespawning strategies, respectively. Moreover, Nesis(1996) added four more types of reproductivestrategies named after representative genera. Thecorrespondence between this and our classificationshould be as follows: Nautilus type – polycylicspawning, Opisthoteuthis type – continuous spawning,Octopus type – simultaneous terminal spawning andArgonauta type – continuous spawning. Ecologicalaspects (e.g. oceanographic characteristics) andreproductive traits (e.g. parental care, somaticdecline after spawning, etc.) are included in thesed£efinitions. A designation by genera has the dis-advantage that the reproductive strategy seems to belimited to the species of the representative genus,although in reality such is not the case. For instance,the Octopus-type strategy contains genera as varied asOctopus and Vitreledonella (Nesis, 1996). Indeed,different strategies can be found in different specieswithin a given genus (e.g. Loligo). Moreover, thisclassification of reproductive strategies makes use ofsome reproductive traits that are unknown in manyspecies, for example the spawning sites or whether ornot there is parental care of the eggs. Consequently,to undertake a suitable classification of the re-productive strategy of any species, a thoroughknowledge of its reproductive biology is necessary.

Nevertheless, the three factors (type of ovulation,spawning pattern and growth or no-growth betweenegg batches) proposed in the present paper are notlimited to any specific taxa. Moreover, they do notpreclude the use of any other reproductive orecological aspects of the species, such as those utilizedby Nigmatullin & Laptikhovsky (1994, 1999) andNesis (1996). Even more significantly, the aspectsindicated by these Russian authors could be used tosubdivide the proposed reproductive strategies intomore fine-grained categories. In fact, these newsubdivisions or categories based on some of theabove-mentioned three factors and some otherreproductive traits (e.g. hectocotylus morphology ornumber and size of the eggs) would serve to describe,


in greater detail, the high variability observed in theflexible reproductive strategies of cephalopods(Rocha et al., 1996). Thus, many of the so-calledterminal spawners could be subdivided into ‘ simul-taneous terminal spawners with parental care’, suchas many Octopus species, or ‘ simultaneous terminalspawners without parental care’, as in various squidspecies.

VI. REPRODUCTIVE STRATEGIES AS

ADAPTATIONS TO ECOSYSTEM DEMANDS

Cephalopods are a very ancient and specializedgroup within the Mollusca. They have occupiedpractically all the marine habitats, and extantcephalopods are well-adapted to their ecologicalrequirements (Rodhouse, 1998). Packard (1972)argued persuasively that the evolution of coleoidswas influenced strongly by competition and pre-dation pressures from fishes and marine reptiles fromthe Mesozoic onwards. Nevertheless, the discovery ofcoleoids from the early Devonian (Bandel, Reitner &Stu$ rmer, 1983; Stu$ rmer, 1985) shows that anypredation pressure on the early coleoids may havebeen exerted by such early vertebrates as chondro-steans or placoderms, and perhaps the scenarioproposed by Packard (1972) is questionable. Thereis strong evidence that cephalopods and their chiefpredators (vertebrates) in the sea have been inter-acting behaviourally for many millions of years(O’Dor & Webber, 1986; Packard, 1988; Hanlon &Messenger, 1996). Furthermore, cephalopods playan important role in the trophic web of the marineecosystems (Clarke, 1987; Rodhouse & White,1995). However, cephalopods are molluscs and notfish, although they resemble modern teleosts to anextraordinary extent in their morphology, physi-ology, ecology and behaviour (Hanlon & Messenger,1996). For that reason, the evolution of cephalopodlife cycles seems to be constrained by their peculiarorganisation (Stearns, 1984). For example, theirprotein-dominated nutrition means that storage andfunctional tissues overlap, so that retrieval ofnutrients from somatic stores for reproductivepurposes always has functional consequences (O’Dor& Wells, 1987; Lee, 1994). On the other hand,cephalopods have high metabolic rates and highgrowth rates and usually produce the numeroussmall offspring associated with this strategy (Calow,1987). Moreover, cephalopods are limited in com-peting directly for restricted resources with pelagicfish because of the inherent limits of jet propulsion on

the maximum sizes and speeds attainable and theensuing energetic cost (O’Dor, 1998a). However,cephalopod reproductive strategies and life-cyclesare genetic adaptations to optimise the use ofecological niches in direct competition with otherspecies, as responses to the environmental conditions.

The high variability and great flexibility of theextant cephalopod reproductive strategies has beenanalysed by considering their life-history patterns(Boletzky, 1986; Mangold et al., 1993; Nesis, 1996)and ecological factors (Nigmatullin & Laptikhovsky,1994, 1999; Nesis, 1996; Laptikhovsky, 1998).Obviously, evolution has proceeded providing manysuccessful adaptations. Boletzky (1986) posed thequestion ‘selection of what? ’, and he emphasisedthat attention must be given to the wide range ofvariation within the major component of repro-ductive effort (fecundity), and to the direct andindirect consequences of fecundity fluctuations.Iteroparous patterns established under aquariumconditions are not necessarily patterns used at alltimes under natural conditions, but the capacity tospawn repeatedly may be the safety factor favouredby natural selection in certain contexts of adaptation(Boletzky, 1986). The capacity to spawn repeatedly,which is the most typical reproductive pattern forsquid, allows annual squid stocks to achieve thediversity and stabilisation that fish stocks (generallyiteroparous) obtain by conserving genetic diversityand stabilizing recruitment through numerous co-existing year classes. In the case of squids, themicrocohorts spawned throughout the year aredispersed widely in space, finding microhabitatswith equivalent variability to those found by the fishlarvae of each year class, which have survived undera wide range of potentially limiting conditions(O’Dor, 1998b).

On the other hand, Russian authors analysed eggdimensions, potential and relative fecundity, theproportion of vitelline oocytes, and peculiarities ofmaturation of the female reproductive system in theOmmastrephidae (Nigmatullin & Laptikhovsky,1994, 1999) and egg dimensions in octopods(Laptikhovsky, 1998, 1999) in relation to r- and K-selection in life-cycles (MacArthur & Wilson, 1967;Pianka, 1970). In ommastrephid species anenhanced K-strategy is peculiar to the shelf-slopespecies and a pronounced r-strategy to the oceanicspecies. According to Nigmatullin & Laptikhovsky(1994, 1999), this corresponds to an evolutionarytrend within the family: the evolution and expansionfrom initial slope-shelf biotopes to oceanic epipelagicones, termed ‘oceanisation’ (Nigmatullin &


Laptikhovsky, 1999). On the contrary, octopodsevolved from the initial ‘position’ of moderatefecundity and egg size in two opposite directions : the‘planktonic ’ strategy (r-strategy), with high fec-undity and small eggs, and the ‘benthic ’ strategy(K-strategy), including low fecundity and largeeggs, with few species occupying an intermediateposition (Laptikhovsky, 1998). The high flexibilityand specialisation in cephalopod reproductivestrategies represents adaptations to survival indifferent environments, fluctuating or not, in directcompetition with fish species.

In analogy to the Russian studies, one can considerthat polycyclic and continuous spawning strategiescould be adaptive responses to stable and ‘safe ’environments, where predation pressure and com-petition for resources may be very low. In suchenvironments, spawning can be slow and continuous,with a limited number of eggs per clutch. Thepolycyclic-spawning species of Nautilus live in a vastwarm-water area, spawning at between 80 and100 m depth in a very stable environment wheretemperatures always range between 21 and 25 °C(Ward et al., 1984). The continuous spawnersOpisthoteuthis agassizii and Opisthoteuthis vossi live inbenthopelagic habitats where the environment isquite stable (Villanueva, 1992). In some cases,however, this ‘ stable environment’ can be createdby the cephalopod itself, as in Argonauta spp., wherethe female guards the eggs within an incubatorstructure (or brood ‘shell ’) until paralarvae hatch(Nesis, 1977).

Conversely, multiple, intermittent terminal andsimultaneous terminal spawning seem to be adap-tations to very unstable environments where a highrate of paralarval survival depends on favourable,but fortuitous and temporary, oceanographicconditions. This occurs in areas with high primaryproduction, which are located in oceanic fronts andupwellings (Trites, 1983; Dawe & Beck, 1985;Parfeniuk, Froerman & Golub, 1992; Saito &Kubodera, 1993; Gonza! lez, Trathan & Rodhouse,1997; O’Dor, 1998a ; Bower et al., 1999; Rocha et al.,1999). These strategies should allow cephalopods totake advantage of any excess production in anecosystem. As noted by O’Dor (1998a) : ‘voraciousfeeding and rapid growth allow squid to grow atabout the same rate as energy moves up through thefood size-spectrum’. During their growth, cephalo-pods can compete successfully with fish from variousyear-classes with varying degrees of effectiveness(Hanlon & Messenger, 1996; O’Dor, 1998a). Prob-ably, the degree of environmental stability reflects

the differences among these three reproductivestrategies. Nigmatullin & Laptikhovsky (1994) linktwo of their reproductive strategies (offshore or Illex

type, and oceanic or Sthenoteuthis type) to spawningevents, which they suppose to occur in the offshoreside of boundary currents. The difference betweenthese two strategies is that in the ‘offshore strategy’,corresponding to our intermittent terminal spawningstrategy, spawning occurs near to, or on the bottomof the continental shelf or slope, whereas in theoceanic strategy, corresponding to our multiplespawning strategy, spawning is not associated withthe bottom but is completely pelagic. The specieswith simultaneous terminal spawning seem to benektonic, such as Loligo opalescens (Hixon, 1983), orbenthic, such as several species of octopods (VanHeukelem, 1983; Nesis, 1996). Todarodes pacificus

pacificus, whose spawning pattern is clearly sim-ultaneous terminal (Ikeda et al., 1993), is anepipelagic-mesopelagic neritic species that lives onthe continental shelf and breeds inshore near thebottom (Okutani, 1983). However, hatching andparalarval growth occur in fronts of the KuroshioCurrent where primary production is high (Bower et

al., 1999).

VII. CONCLUSIONS

Living cephalopods have developed a wide array ofreproductive strategies showing a high adaptiveflexibility. The reproductive options of coleoids,usually short-lived animals, extend from massive andsimultaneous spawning at the end of the animal’s lifeto continuous spawning during long portions of theirlife-spans.

The five reproductive strategies defined in thispaper encompass all the reproductive patternspreviously described by cephalopod workers.Definitions of these reproductive strategies are basedon only three features : ovulation pattern, spawningpattern and whether or not growth occurs betweenspawning events (Fig. 1). These five reproductivestrategies can accommodate the reproductive style ofany cephalopod species. This is an open classi-fication, which allows the incorporation of additionalfactors, like parental care, egg size, fecundity, etc.,facilitating any envisagable splitting of the fivebroad groups into more specific categories.

Moreover, this classification permits ecologicalexplanations of the reproductive strategies as suc-cessful adaptations of each species to differentenvironmental and demographic pressures acting


Fig. 1. Diagram illustrating the five cephalopod reproductive strategies in relation to the type of ovulation, the spawn-ing pattern and whether or not somatic growth between egg batches occurs. These strategies are adapted to a givendegree of environmental stability, as successful adaptations of each species to the different environmental and demo-graphic pressures faced during evolutionary processes.

during evolutionary processes. Nevertheless, it is notyet clear why cephalopods have evolved such variedand complex reproductive systems. The answer tothis question could be related to the physiologicalinvestment for growth and reproduction (Calow,1987). From a behavioural viewpoint, however,much of the response to this question is constrainedby the concept of reproductive success, whichmeasures fitness in terms of number of progeny thatare produced in successive generations (Hanlon &Messenger, 1996). The actual measurement ofreproductive success in cephalopods has not yet beenaddressed by anyone.

VIII. ACKNOWLEDGEMENTS

We thank our colleagues Drs M. Rasero, T. Cortezand B. G. Castro of the ECOBIOMAR researchgroup at the Instituto de Investigaciones Marinas(CSIC) for their valuable comments provided duringthe constructive discussions held while this paperwas in preparation. We are indebted to Drs E. G.

Dawe (Department of Fisheries and Oceans, St.Johns, Canada), M. Vecchione (NHFS NationalSystematics Laboratory, Washington, DC, USA),K. N. Nesis (P. P. Shirshov Institute of Oceanology,Russian Academy of Sciences, Moscow, Russia) andan anonymous referee for their critical comments onthe manuscript. We would also like to thank Dr J. B.Wood for helpful suggestions made on an early draftof this manuscript.

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A review of reproductive strategies in cephalopods

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