Physiological Progenesis in Cephalopod Molluscs

4 Pages·1998·1.7 MB·English

by  P G Rodhouse

Reference: Biol. Bull. 195: 17-20. (August, 1998)
Physiological Progenesis in Cephalopod Molluscs
PAUL G. RODHOUSE
British Antarctic Sun'ey, Natural Environment Research Council, High Cross, Madingley Road,
Cambridge CBS 9BG, UK
The coleoid cephalopods (cuttlefish, squid and octo- maturation is accelerated while other aspects of the
pus) arosefrom their shelled ancestors during the late physiology are more typical ofthejuvenile.
Devonian: the\ diversified in the Jurassic but did not The life cycle of most benthic marine molluscs (bi-
radiate substantially until the Tertiary. Since then they valves and gastropods) is characterized by a relatively
have coevolved with the fish (I). Squidare less efficient short egg and larval stage, a long adult life span (usually
energetically than fish (2) but have survived alongside several years), and iteroparity (8). Feedingrates ofherbiv-
them by evolving highly opportunistic reproductive and orous and carnivorous species decline relative to body
feeding strategies (3, 4) as well as rapid jetting and mass overthe lifetime, and the mass exponent for feeding
inkingfor escape anddefense. Little is known about the rate is invariably less than for metabolic rate (9). These
life historv strategies of the fossilforms, but the only allometric relationships between consumption rate, meta-
surviving shelled cephalopods, the nautiluses, have rel- bolic rate, and body mass mean that, as body size in-
ativelv long life spans and are iteroparous; that is, in creases, theamountofenergyproducedby foodconsump-
common with most members ofothermolluscan classes, tion decreases relative to the amount of energy lost as
they breed more than once during their lives. In con- heat. The relative scope for growth therefore decreases
trast, all other living cephalopods are generally short with size, and this is the physiological basis forthe stead-
lived(usually I year)andhave monocyclicreproduction ily decreasing gross and net growth efficiency with age
and a semelparous life history. The short-lived semel- (10). Annual production ofsomatic tissue reaches a maxi-
parous coleoids are typifiedby the mid-latitude ommas- mum during the first half of the life span and declines
trephidsquid whichprovide the basic model considered thereafter, whereas gamete production increases asymp-
here. Thisfamily is relativelyprimitive and biologically totically. Somatic production exceeds gamete production
wellknown. Its membersare essentially monocyclic. but during early life, but is later exceeded by gamete produc-
some species may spawn their eggs in batches (5, 6), tion, which eventually dominates tissue growth. Lifetime
although there is no evidence of this in laboratory energy budgets have been estimated for some bivalves
spawnings (7). Most loliginid squid, at least in temper- and gastropods (11, 12), and the general pattern ofenergy
ate seas, have a life cycle similar to that ofthe ommas- allocation is illustrated in Figure la. Lifetime energetics
trephids, despite having different spawning habits. A is dominated by respiratory losses in the form of heat. A
comparison ofthe lifetime energetics and growth pat- substantial proportion of total production is allocated to
tern ofbenthic, iteroparous molluscs with those of the shell organics, and this, together with the energy cost of
pelagic, semelparous ommastrephids shows that, al- mineralization (13), reduces the energy available for tis-
though some squid ma\ attain a length of I m or more, sue growth in these benthic forms.
the allocation of their energy resource among growth The physiological energetics ofNautilus, which proba-
components isessentiallycharacteristic ofthe early life, bly resembles that of the ancestors of the living coleoids
especially the first year, ofiteroparous forms. The life- in many respects, differs substantially from that of the
time energy budget of these squid thus seems to have coleoids with respect to reproduction (14). Nautilus has
evolvedbyphysiologicalprogenesis, aprocess in which a life span of more than 4 years, and its reproduction is
iteroparous, so in many respects its lifetimeenergy budget
resembles that of the iteroparous benthic molluscs.
Received 4 February 1998; accepted 27 May 1998. Relative to most iteroparous molluscs, including Nauti-
E-mail: [email protected] lus, the life cycle ofthe semelparous cephalopods is char-
17
18 P. G. RODHOUSE
a) respectively (9). The massexponentformetabolic rate has
long been thought to be close to 1.0 in small organisms
100 (< 50 mg) and approaching 0.75 in largerones (17). This
exponent has been suggested to derive from the weighted
sum of body surface area and volume (18). Squid appear
to fall between the predicted values for large and small
organisms. The exponent for feeding rate is lower than
for metabolic rate, but the difference between these expo-
nents in the /. illecebrosus example is less than in the
longer-lived iteroparous molluscs (9). implying relatively
Metabolic heat loss (respiration) higher scope for growth at larger body size in the squid.
This is reflected in relatively high growth efficiencies
(15). Somatic tissues grow for most ofthe squid life span,
but gonad growth is rapid once sexual maturation is initi-
L0cU1 ated. Illcx ur^entinus, with a life span of about a year,
starts to mature in about 7 or 8 months and reaches full
maturity by 12 months ( 19). Lifetime production ofsoma
and gonad in /. argentinus has been estimated from data
Production (shell organics) on growth and allometry combined with biochemical
composition (19, 20). The pattern of energy allocation
Production (soft tissue) among soma and gonad in the squid differs fundamentally
from the pattern in the long-lived iteroparous molluscs
10 15 20 (Fig. Ib). Production ofsomatic tissue continues until full
sexual maturity; and even in the latter part of the life
1000 span, when the squid isreaching maturity, somatic growth
remains in excess of gonad production. This pattern of
energy allocation among soma and gonad closely resem-
Production bles that of the first year of the longer-lived iteroparous
molluscs. Suitable data on lifetime metabolic heat losses
in cephalopods are not available for comparison with the
benthic forms.
The declining relative scope for growth and increasing
allocation of energy to reproduction is the mechanism
underlying the form of the asymptotic growth curve fol-
lowed by these longer-lived iteroparous molluscs. The
von Bertalanffy growth function is commonly used in
ecology and fisheries science to model asymptotic growth
of animals (21 ) and has provided an adequate fit to most
data for annual growth increments in iteroparous mol-
Years luscs. The equation is generally given as:
Figure 1. Energy, in kilojoules (kJ). allocatedtothedifferentcompo-
nentsofgrowthandmetabolism: (a)overthe20-yearlifetimeofa long-
lived, iteroparous benthic bivalve (OstreaediilisY, (b)overtheone-year
lifetime ofa short-lived semelparous cephalopod (lllex argentinus). in which 1, is length at time t, Lx is length at infinite age,
K is the rate constant at which L:,: is approached, and t,,
is effectively a scaling factor that displaces the curve
along the age axis to fit the data. Seasonally of growth
aacntderbiyzeda bsyhorltonagduelgtg,lifpea.raFleaervdailn,gaannddjumveetnaibloelipcharsaetse,s has also been modeled by substituting day-degrees for
time in the von Bertalanffy model (22. 23):
are higher than in other molluscs (15), and empirically
determined mass exponents forfeeding and metabolic rate
are higher than in benthic molluscs 0.79 [feeding] and
0.96 [metabolism] for the squid lllex illecebrosus (16) in which 1,, is length at D day-degrees, KD is the rate
c0.o7m0pare0d.1w3it[hmemteaabnolivsalmu]esfoorf306.5a8nd 500.1b2en[tfheiecdisnpge]ciaensd. cdoanys-tdaengtredees)tearnmdinDe,d, =astK-/DDry T(hDiysimsotdheelsantnhuealeffseuctms ooff
PHYSIOLOGICAL PROGENESIS IN CEPHALOPODS 19
seasonal temperature variation only and not, forexample, to morphological phenomena (paedomorphosis) (31).
changes in food available to suspension feeders grazing applying the concept ofprogenesis to physiological ener-
on seasonal phytoplankton blooms. The von Bertalanffy getics provides a useful insight into the evolution of pat-
model rarely, ifever, fits growthduring thejuvenile phase terns of cephalopod growth and reproduction.
(usually the first year oflife), hence the necessity for the For much of their life span, squid occupy the juvenile
mathematical convenience of the term t , as the fitted phase of the generalized molluscan life cycle that is not
model rarely passes through the origin. The poor fit of readily fitted by the von Bertalanffy growth function. Be-
the von Bertalanffy function to growth of the juvenile cause this function rarely fits the growth data for squid
phase is probably due tothecombined effects ofseasonal- orother cephalopods (32), they have been compared with
ity of growth in the first year and different patterns of larvae ofother taxa that do not grow asymptotically (33).
energy allocation during the pre-reproductive phase of If, as has been argued, the von Bertalanffy function is
early development. fundamentally applicable to squid (34), they probably die
The high growth efficiency ofsquid, togetherwith their before, or very soon after, approaching the asymptotic
relatively low investment in gonadal growth, results in phase. The principal factors that underlie the complicated
high growth rates throughout the life span (24). This effi- and highly variable growth trajectories ofthese molluscs
ciency is accentuated by their semelparity. because the are changes in the allocation ofenergy resources between
reduction in growth rate, due in iteroparous forms to the soma and gonad: seasonality of growth rate, modulated
energetic costs of repeat spawning, is not experienced. by food availability andtemperature; andthe confounding
The age of ommastrephids taken from the field has been effects of hatching season on lifetime growth rate. The
estimated from daily growth increments in the statolith. underlying lifetime pattern of energy allocation and the
These data show that growth in mantle length of adults consequentgrowthcharacteristicsofthecephalopods sug-
up to sexual maturity can generally be fitted by a simple gest that these traits have evolved through physiological
linear model ( 19, 25). But there are no data covering the progenesis, in which sexual maturation has been acceler-
whole life span of ommastrephids, including the brief ated, while the energy budget retains features found in
post-spawning phase, so the form of the growth curve the juvenile phase of other classes of molluscs.
towards the end oflife is not known. The allometric coef-
ficient in ommastrephids is generally close to 3.0 (24). Acknowledgments
dinsneoitetmadhiaelbseylsdinamieseaparbosepwsuhetraresfmeicteutonerfdtvgsebryhroeawfavtlnehecebitxniepnemognannegmtnraltoiedwaetllheongnigrntoshmwqaiutssihdsa,.cfcugWnorhcmotepwirato-ehn midaeIdaesthdnaonukwmenDraoonnuiseplahpePleaprufluaylndcfortrihteiecniacsnomous.rnaygmionugsmreevtioewgeertstwhehsoe
forearly life and a powerfunction forthe latter phase (24,
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