Understanding the process of growth in cephalopods

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Marine and Freshwater Research, 2004, 55, 379–386

Review

Understanding the process of growth in cephalopods Natalie A. Moltschaniwskyj School of Aquaculture, Tasmanian Aquaculture and Fisheries Institute, University of Tasmania, Locked Bag 1370, Launceston, Tas. 7250, Australia. Email: [email protected] Abstract. Many cephalopod species grow throughout their lifetime. Critically, this means that they lack an asymptotic phase of growth, when, for a substantial part of the lifetime, growth slows and body size increases minimally. Understanding the form of the growth curve requires an understanding of the growth processes operating at several biological levels including the relative growth of organs, muscle fibre production and growth, and at the level of proximal composition and protein synthesis. There are key differences in growth processes between fish and cephalopods; cephalopods have a sac-like body form that provides greater surface area for respiration, continuous production of new muscle fibres that ensures a supply of somatic material for growth, and high retention of synthesised protein. These characteristics provide process-orientated explanations for non-asymptotic growth in cephalopods. However, differences found in growth curves of laboratory-reared animals (two-phase growth curve) and of wild animals (single growth curve) suggests that future work will be needed to resolve this paradox. We need to determine the generality of growth processes observed to date, and how biotic and abiotic factors modify these processes during the lifetime of the animals. Extra keywords: muscle fibres, proximal composition, relative growth, reproduction, whole animal.

Introduction Growth of an individual, the increase in length or biomass, is an important measure in ecology. Rates of growth are indicators of resource availability and an assessment of the condition of individuals and the environment. Growth, measured at the whole–animal level, is the change in total length or biomass through time. Size-at-age data provide an estimate of the rate at which size increases and how this rate changes as a function of mass, age, and condition (somatic and reproductive). Fitting equations to size-at-age data can be generated either as mathematical descriptions used for predictions (e.g. in population modelling), or as a description of a biological process. However, there is an assumption that the use of growth equations is based on a premise that physiological processes underlying the growth process are understood. Growth is a complex process that occurs on many biological levels, which can be viewed hierarchically and includes changes in the relative size of organs, the generation and growth of muscle fibres, and the physiological process of synthesising protein (Ho et al. 2004). Therefore, understanding the form of lifetime growth curves and how biotic and abiotic factors, such as temperature and food, alter growth rates will only occur by understanding processes at lower levels of organisation (Weatherley 1990). © CSIRO 2004

As a general rule, most squid grow throughout their lifetime and attain a maximum body size very shortly before senescence (Jackson 1994). As a result, the asymptotic phase of growth, which is a dominant feature of the life history of most molluscs and teleost fish, is absent or very short in many coleoid cephalopods. This is often the case when non-asymptotic growth models are fitted to size-at-age data (Arkhipkin and Fetisov 2000). The shape of the growth curve is a function of the metabolic and energetic demands of biological processes that typically change with body size (Pauly 1998). Generation of protein is a major process contributing to oxidative metabolism (Houlihan et al. 1993) and oxygen uptake is non-linearly related to body size, therefore growth will slow as body size increases. In the cephalopod literature there is conflict between laboratory and field studies over the degree to which growth slows and the rate at which growth slows. For example, growth of the Indo-Pacific squid Sepioteuthis lessoniana slows during the lifecycle in captivity (Forsythe et al. 2001), however, size-at-age data obtained from wild populations fails to detect this (Jackson and Moltschaniwskyj 2002). However, in a direct comparison of wild and laboratory-reared individuals of this species there was no difference in the form of the growth curve (Jackson et al. 1993). 10.1071/MF03147

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Pauly (1998) noted correctly that observing and describing non-asymptotic growth (see review by Jackson 1994) and physiological progenesis in cephalopods (Rodhouse 1998) does not explain how these phenomena occur. However, they can be viewed as hypotheses that provide a basis and an approach from which process-orientated research can progress. Likewise, Pauly (1998) provided a base upon which the differences and similarities in the processes underlying growth in cephalopods and fish can be explored. The nonasymptotic form of the growth curve has implications for the allocation of energy to somatic growth v. reproductive growth. In teleosts, slowing of growth and attainment of maximum body size is in part attributed to the re-allocation of energy away from somatic growth in favour of stored energy and reproduction (Wootton 1990). Assessing changes in somatic tissue structure and composition during starvation provides an insight into how and where energy is allocated during periods of high energy use, and the effect of feeding levels on variability of growth. Growth estimates for many cephalopod species reveal considerable variability in size for a given age, particularly in adults (Jackson et al. 1997; Pecl 2000; Arkhipkin 2004; Jackson 2004). Much of this variation is a function of temperature (the ‘Forsythe Effect’, Forsythe 1993, 2004). This has been observed in laboratory experiments (Forsythe et al. 2001) and is suggested to be the major factor driving differences in seasonal growth rates of wild individuals (Jackson and Moltschaniwskyj 2002). Also important in driving this variability are food intake (Koueta and Boucaud-Camou 1999), sexual maturation (Brodziak and Macy 1996), and gender (Arkhipkin et al. 2000). These factors modify rates of growth at lower hierarchical levels because whole-animal growth is a function of growth at lower levels (Weatherley 1990). When food intake, sexual maturation and gender interact, the growth response is difficult to predict because these factors can alter the processes of growth. Assessing growth at different biological levels is undertaken for a variety of reasons. At the whole-animal level, growth rates are used for population biomass estimates and in predictive tools of temporal changes in biomass. Spatial and temporal changes in growth rates provide a basis on which to understand and determine biotic and abiotic factors responsible for variation in growth rates. At lower levels of biological organisation, describing growth through the size–frequency distribution of muscle fibre and estimates of protein synthesis allow us to validate the form of the growth curve. This in turn allows an understanding of how the processes of growth change as a function of size and age. This review examines what is known about how growth occurs in cephalopods and what we currently understand about how starvation and sexual maturity affect growth processes to produce the form of the growth curve. Currently, our knowledge is limited to those squid, cuttlefish and octopus species that are of commercial interest or are

N. A. Moltschaniwskyj

relatively common. Little is known about some of the large species or those that occupy extreme environments such as deep water. This review should provide a basis for our understanding against which these species can be compared and contrasted. Assessment of growth Relative growth of organs Changes in the relative size of organs during growth are generally conserved features, ensuring functionally of the whole animal. Relative growth of organs is usually allometric in juveniles and isometric during the adult growth phase. However, differences in allometric growth as a function of factors such as gender, nutrition, and temperature, provide information about energy allocation to organs throughout their lifetime. The relationship between length and weight is an indicator of somatic condition in both teleosts and some cephalopods (squid and cuttlefish). Octopods do not have a skeletal-type hard structure, which prevents reliable measures of body length. Use of somatic condition assumes that individuals heavier for their length are in better condition than individuals lighter for their length. Condition indices may be indicators of health, nutritional status, and evolutionary fitness (Hayes and Shonkwiler 2001). Descriptors of whole-animal condition commonly used are ratios (e.g. Fulton’s K) and residuals from regressions. The validity and problems associated with condition measures are discussed by several authors (García-Berthou 2001; Hayes and Shonkwiler 2001) The volume and surface area relationships of cephalopods differ dramatically from teleosts because they are hollow tubes or sacs rather than solid bodies. Pauly (1998) argues that squid growth should be asymptotic, because, like fish, the surface area available for oxygen uptake should decrease as volume increases. However, physiological and morphometric data do not support Pauly’s assertion. Modelling growth allometries from six squid species suggests that surface area does not converge with volume (O’Dor and Hoar 2000). Furthermore, in octopus, cutaneous respiration accounts for 41% of oxygen uptake (Madan and Wells 1966). Therefore, there is little support for the argument that increasing mass in cephalopods should result in asymptotic growth (O’Dor and Hoar 2000). Changes in the relative size of organs of starved individuals indicate where energy reserves are stored for reproduction and migration. Starved Octopus vulgaris undergo marked changes in mantle muscle and digestive gland mass (Tait 1986). Likewise, starved cuttlefish, Sepia officinalis, undergoes an immediate and dramatic decrease in digestive gland lipids and eventually the mantle muscle loses protein (Castro et al. 1992). Therefore, when energy demand is high, changes in the relative mass of the digestive gland and mantle muscle occur as stored energy is used. An extreme example

Processes of growth in cephalopods

of this is the severe deterioration of mantle muscle associated with reproduction suggesting that protein is mobilised as an energy source (e.g. Moroteuthis ingens, Jackson and Mladenov 1994; Moroteuthis robsoni; Chaunoteuthis, Voss 1983). Less dramatic changes are seen as a decline in relative mass of the mantle during reproductive maturation of squid (e.g. Illex argentinus, Hatfield et al. 1992; Photololigo sp., Moltschaniwskyj and Semmens 2000) or slowing somatic growth in the squid Photololigo sp. (Moltschaniwskyj 1995). These subtle differences suggest that energy for reproduction is sourced directly from ingested food and not from stored reserves (Hatfield et al. 1992; Moltschaniwskyj 1995). Changes in the relative mass of the digestive gland were evident in female I. argentinus (Hatfield et al. 1992), but not in Photololigo sp. (Moltschaniwskyj and Semmens 2000), possibly indicating different roles of the digestive gland. Growth dynamics of muscle tissue Growth at the whole-animal level is driven by growth processes at the level of the organs. Muscle tissue accounts for much of the body mass in many cephalopods and increases in mass by two processes: hyperplasia (generation of new muscle fibres) and hypertrophy (increase in fibre size). In fish, hyperplasia ceases as individuals approach final body size and growth occurs through hypertrophy only, however maximum fibre size is limited physiologically. As a result, maximum body size and the very slow growth associated with the asymptotic phase are because growth occurs only by hypertrophy (Weatherley 1990). Cephalopods do not show the same pattern of changes in the relative rates of hypertrophy and hyperplasia during their lifetime as fish. In cephalopods examined to date, the squid species Photololigo sp. (Moltschaniwskyj 1994), Loligo opalescens (Preuss et al. 1997), Sepioteuthis australis (Ho et al. 2004), and Nototodarus gouldi (McGrath Steer 2003), the sepioid Idiosepius pygmaeus (Pecl and Moltschaniwskyj 1997), the cuttlefish Sepia elliptica (Martínez and Moltschaniwskyj 1999), and Octopus pallidus (Hoyle 2002), small muscle fibres are present in individuals irrespective of size or age. Only for the tropical squid Photololigo sp. and cuttlefish S. elliptica is muscle fibre data available across a full range of size, age, and somatic and reproductive conditions. Wildcaught adults (Photololigo sp., I. pygmaeus, L. opalescens, and N. gouldii, S. elliptica, Sepioteuthis australis) all have small muscle fibres present. Laboratory-maintained individuals growing at time of death also had small muscle fibres present (Sepia elliptica, I. pygmaeus, and L. opalescens). Therefore, new fibre production continues throughout the lifetime of individuals and, as a result, final body size of cephalopods is not limited by the number of fibres produced. Structural and metabolic differentiation of muscle tissue is evident in a range of species (Moltschaniwskyj 1994; Pecl and Moltschaniwskyj 1997; McGrath Steer 2003). An


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inner and outer zone of mitochondria-rich oxidative fibres is most likely used for slow steady-state swimming and respiratory movements, while a central region of mitochondria-poor glycolytic fibres may be used for rapid movements and burst swimming associated with prey capture and predator avoidance (Mommsen et al. 1981). The majority of muscle fibres in the mantle are mitochondria-poor and are more than an order of magnitude smaller than fish fibres (Hanson and Lowy 1957; Bone et al. 1981), but comparable in size to other molluscs (e.g. Haliotis spadicea, Frescura and Hodgson 1992). Given the size of small fibres, increases in body mass will require rates of hyperplasia to be greater than hypertrophy and therefore hyperplasia will be a major determinate of growth rates (Preuss et al. 1997). The size frequency distribution of the fibres allows us to determine the relative importance of hyperplasia and hypertrophy but not the absolute rates of these two processes (Rowlerson and Veggetti 2001). Factors influencing the relative importance of hypertrophy and hyperplasia in growth vary among species. In both the sepioid I. pygmaeus (Pecl and Moltschaniwskyj 1997) and squid Photololigo sp. (Moltschaniwskyj 1994), hyperplasia is relatively less important in the growth of larger individuals. The squid Sepioteuthis australis (Semmens and Moltschaniwskyj 2000), and cuttlefish Sepia elliptica (Martínez and Moltschaniwskyj 1999) both displayed constant relative rates of fibre growth and recruitment as body size increased. In contrast, in O. pallidus (Hoyle 2002; Semmens et al. 2004) new fibre production is relatively more important in the process of muscle growth. The relative rates of hypertrophy and hyperplasia are highly context dependent. In the tropical sepioid I. pygmaeus the dynamics of muscle growth differed between wild and captive individuals (Pecl and Moltschaniwskyj 1999). Within 7 days of captivity, changes in the relative rates of fibre production and growth were evident. Furthermore, structural changes to the fibres and the amounts of mitochondria-rich tissue had also occurred. Therefore, factors associated with captivity (e.g. stress, food intake, and limited movement) potentially modify cellular growth processes rather than simply altering the physiological rates of growth. Similarly in laboratory experiments, both temperature (Hoyle 2002) and ration (Moltschaniwskyj and Martínez 1998) change relative rates of fibre production and growth. However, how the processes of growth are affected depends upon the factor responsible and the species being investigated. In the tropical cuttlefish S. elliptica temperature affects growth by altering the absolute rates of fibre production and growth, while ration altered the relative rates of fibre production and growth (Moltschaniwskyj and Martínez 1998). In contrast, the temperate octopus O. pallidus (Hoyle 2002), when held in either increasing or decreasing temperatures, displays greater relative rates of hyperplasia that individuals grown in constant water temperature. Currently, it is unclear what the lifetime consequences, with respect to the form of the

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Table 1. Biochemical correlates with growth for a range of cephalopod species Species Sepia officinalis Sepia officinalis Sepia officinalis Sepia elliptica Euprymna tasmanica Eledone cirrhosa Octopus vulgaris Octopus vulgaris Loligo forbesi Sepioteuthis lessoniana Sepioteuthis australis

Biochemical measure RNA : DNA Asparate transcarbamylase RNA RNA : protein RNA : protein RNA : protein Muscle RNA RNA and RNA : protein RNA and RNA : protein RNA : protein RNA : protein

Correlated with growth? 17.5◦ C,

Yes at no at Yes, early growth Yes, early growth No Yes Yes Yes, recent growth No No Yes No

growth curve and the body size, are when the relative rates of hyperplasia and hypertrophy are altered. It is possible that small changes in rates of these processes have the potential to generate differences in size-at-age of the magnitude predicted by temperature (Forsythe 1993). Complete histolysis (breakdown in muscle fibres) of the mantle tissue associated with maturation does occur in some squid, for example, the oceanic squid Moroteuthis ingens (Jackson and Mladenov 1994). In contrast, species with no or small differences in somatic condition associated with maturation have correspondingly little or no change in the structure or organisation of the muscle fibres and growth appears to continue (e.g. Illex argentinus, Hatfield et al. 1992; Sepioteuthis australis, Ho et al. 2004). This provides further evidence that stored protein reserves are not fuelling reproduction. Where relative rates of fibre production and processes of growth did change during maturation, for example, in the squid Photololigo sp., maturing females had relatively slower rates of fibre production, and ovulated females had either increased rates of hyperplasia or resorption of fibres (Moltschaniwskyj 1995). Such changes in the fibre production and growth subsequently result in slower growth in mature Photololigo sp. Proximal composition and biochemical measures Cephalopods, like fish, change their body mass by the processes of protein accretion and degradation that underlie growth. Therefore, relative rates of protein accretion and degradation as a function of body size and age allow further exploration of the hypothesis of non-asymptotic growth. Rates of protein synthesis are difficult to quantify directly, therefore indirect measures are frequently used. Protein synthesis is a function of the number and activity of ribosomes in the tissue and ribosomes contain the majority of RNA. In octopus, there is a linear relationship between RNA concentration and fractional rates of protein synthesis (Houlihan et al. 1990). Hence, RNA concentration expressed as a ratio of RNA to protein can be used as a measure of the capacity or potential for protein synthesis and growth (Houlihan et al. 1993). In the cephalopod literature, RNA has also been

12◦ C

Reference Clarke et al. (1989) Koueta and Boucaud-Camou (1999) Koueta et al. (2000) Moltschaniwskyj and Jackson (2000) Fox-Smith (2002) Houlihan et al. (1990) Houlihan et al. (1998) Pierce et al. (1999) Pierce et al. (1999) Moltschaniwskyj and Jackson (2000) Ho et al. (2004)

expressed as a concentration as well as ratios with DNA and fresh weight (Table 1), although RNA : DNA is problematic in teleosts (Houlihan 1991). A more direct assessment of protein synthesis has been explored through the measurement of enzymes involved in nucleic acid synthesis, for example, aspartate transcarbamylase (Koueta and BoucaudCamou 1999; Koueta et al. 2000), or quantifying the rate that labelled amino-acid becomes incorporated into body tissues (Houlihan et al. 1990). RNA concentration as a measure of growth is being explored as an alternative to estimating growth rates from size-at-age relationships by cephalopod biologists and ecologists. This is largely because statolith microstructure cannot be used to determine age in some species, but also to estimate instantaneous assessments of growth rather than lifetime estimates. The success of biochemical alternatives for estimating growth rates in cephalopods has been mixed (Table 1). In some studies there have been correlations between these measures and feeding rates (Koueta and Boucaud-Camou 1999; Pierce et al. 1999) and subsequently a correlation with growth rates. However, this outcome is not universal (Table 1) with many studies finding correlations only with recent growth (Houlihan et al. 1998). Protein concentration is highly variable (Pierce et al. 1999; Moltschaniwskyj and Semmens 2000; Semmens and Moltschaniwskyj 2000), suggesting that the RNA : protein ratio may not provide a reliable measure of growth rates, but that protein concentration by itself may (Pierce et al. 1999). As growth rates ultimately are a function of the relative rates of protein synthesis and degradation, when rates of protein degradation are slow, the retention of protein for growth is greater (Houlihan et al. 1993). In O. vulgaris ∼90% of synthesised protein is retained (Houlihan et al. 1990), which is relatively large compared with fish (e.g. 40% in cod Gadus morhua, Houlihan et al. 1988), but similar to other molluscs (e.g. 95% in the mussel Mytilus edulis, Hawkins 1985).This poses the question of whether the growth rates observed in cephalopods are a function of their molluscan heritage, rather than a response to the cephalopod lifestyle. The next step to fully understanding the form of the


growth curve will be to assess rates of protein synthesis and retention throughout the lifetime of individuals. A prediction from the hypothesis of asymptotic growth in cephalopods is that retention of synthesised protein is high throughout their lifetime. Understanding patterns in changes in somatic condition and digestive gland condition associated with starvation and reproduction (see earlier sections of this review) can be explored through the composition of the tissues. Stored protein in the mantle muscle may be an energy source for some cephalopods (O’Dor and Wells 1978; Jackson and Mladenov 1994; Pierce et al. 1999). Captive L. forbesi that lost weight may have been metabolising body protein (Pierce et al. 1999), given that water content increased and protein concentration decreased in the mantle muscle of starved cuttlefish S. officinalis (Castro et al. 1992). The allocation of energy from somatic to reproductive growth is typically associated with slowing growth and decreased potential for growth. Both L. forbesi and Eledone cirrhosa show a consistent pattern of higher levels of RNA : protein in immature individuals than mature individuals (Pierce et al. 1999). Furthermore, the same study found mature males had a greater potential for growth than mature females, indicating that the cost of reproduction is greater for females than males. These patterns were consistent for both wild and captive individuals. Compared with other molluscs glycogen reserves in cephalopod muscle tissue are very low (Suryanarayanan and Alexander 1971). Carbohydrate concentration, the first source of stored energy, is affected by water temperature and ration level in young cuttlefish, suggesting some capacity to store energy in this form (Moltschaniwskyj and Martínez 1998). While there is no evidence of mantle muscle protein being used for maturation in the tropical squid Photololigo sp., females show a reduction in lipid and carbohydrate concentration (Moltschaniwskyj and Semmens 2000). However, in the oceanic squid Illex argentinus there is little change in mantle muscle composition with maturation in either males or females, with the only change detected being carbon in males and nitrogen in females (Clarke et al. 1994). Allocation of energy to somatic tissue still occurs in maturating I. argentinus as evidenced by investment of carbon to somatic tissue (Clarke et al. 1994) and size-at-age data (Rodhouse and Hatfield 1990). This is despite high lipid content of the digestive gland of I. argentinus, which is hypothesised to be stored energy reserves for migrations and final vitellogenesis (Clarke et al. 1994). The role of lipid as a storage product and as an energy source for growth is unclear. Lipid deposits in the digestive gland may be associated with stored energy (Castro et al. 1992) or excretion (Semmens 1998). Relatively high lipase activity in the digestive gland of the dumpling squid Euprymna tasmanica suggests a capability to digest lipid (N. A. Moltschaniwskyj and D. J. Johnston, unpublished


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data). Although lipid and carbohydrate are available as stored energy sources, protein still appears to be the main energy source during starvation (O’Dor et al. 1984; Boucher-Rodoni and Mangold 1988; Segawa and Hanlon 1988; BoucherRodoni 1989). The large muscle mass and highly active lifestyle of cephalopods mean that protein stored as muscle tissue has a dual role and capability in mobility and stored energy. Understanding growth in cephalopods: the story to date If we integrate what is known about growth in the three levels of organisation we start to develop a realistic model of growth based on an understanding of the processes of growth. I will make some generalised comments, which may not be applicable to all cephalopod species, however, it provides the next step to understanding the processes of growth in cephalopods. Some cephalopod species have exponential lifetime growth curves, suggesting no slowing of growth. However, most have growth curves that indicate slowing of growth during their lifetime (see review by Jackson 1994); probably associated with energetic demands of reproduction. This is evidenced by the fact that reproduction appears to be largely fuelled directly and preferentially directly by ingested food, rather than stored energy reserves. Furthermore, potential for growth (measured through RNA) is higher in immature animals and declines with body size and maturation. The absence of an obvious and dominant asymptote phase in the lifetime of many cephalopods can be explained by processes responsible for growth and processes that limit growth (Fig. 1). First, the shape and isometric growth of the squid body does not limit oxygen uptake. Second, somatic growth does not appear to be limited by the production of new muscle fibres, until re-direction of ingested energy is required, which may result in a slowing of growth. Third, the use of protein in muscle tissue as a stored energy product will result in continuous growth. However, there are some clear differences among species, especially with respect to the extent to which protein from the mantle tissue is used as an energy store (e.g. the oceanic squid Moroteuthis and Octopus spp.), which is not seen in many species. The diversity of growth curves being generated to describe size-at-age data is another difference. Such interspecific differences need to be the focus of future work and may relate to environmental and genetic influence of energy use during the final stages of life and relate to senescence events. It is likely that cephalopods have a very short asymptotic growth phase that is associated with senescence (Pauly 1998; Rodhouse 1998). Although this phase is evident in the fitting of linear and power growth curves, it has been difficult to detect in most species (Hatfield 2000), most probably because of variability in size-at-age in adults and the speed of senescence. Likewise contradictions about

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Whole body – body size does not limit oxygen uptake

Form of the growth curve – nonasymptotic

Muscle fibres – continuous production of fibres

Biochemical constituents – high protein retention

Fig. 1. The influence of processes at different levels of organisation that in part explain why it is possible that many cephalopods display non-asymptotic growth.

the form of the growth curve between laboratory and field studies are typical during the final stages of growth, when senescence processes maybe influencing metabolic rates and processes of growth. Given that the growth process can be modified in the laboratory (Pecl and Moltschaniwskyj 1999), laboratory growth experiments need to be interpreted with caution. Frequently, changes at the level of the muscle-fibre dynamics and proximal composition are not directly correlated with changes at the whole-animal level (Moltschaniwskyj and Jackson 2000; Semmens and Moltschaniwskyj 2000; Hoyle 2002). Also observed in teleost species, particularly juveniles (Suthers et al. 1992), this is largely attributed to the differential rate at which processes at different organisation levels respond to biotic and abiotic factors. In other words, size-at-age is a measure of lifetime growth, while rates of protein synthesis will be a function of the immediate nutritional or environmental history of the individual. Both early and late in the starvation period, protein in the muscle tissue supplies most of the required energy in the cuttlefish Sepia officinalis (Castro et al. 1992). Such use of muscle proteins would result in a dynamic system of increasing and decreasing mass depending on the nutritional state of the animal. Such sensitivity to both food levels and temperature would result in considerable variability in size-at-age and protein concentration.

Cephalopods are living life in the fast lane and the processes of growth at the different organisational levels will respond differently to biotic and abiotic conditions. This explains both the observed variability in life-history characteristics and the difficulty of correlating rates of growth processes at different organisation levels. Part of the solution to understanding the process of growth and the variability will be well-structured laboratory experiments that quantify the exact growth trajectory, reproductive, and nutritional history of individuals. Given this information it may be possible to understand how processes at lower organisation levels are expressed at the whole-body level, and to understand how biotic and abiotic factors influence biomass and reproductive output of populations. Acknowledgments This review benefited from many conversations and discussions with several of my colleagues and two anonymous referees. I would like to thank, in particular, Gretta Pecl for her valuable comments and willingness to discuss ideas over the years. References Arkhipkin, A. I. (2004). Diversity in growth and longevity in short-lived animals: squid of the suborder Oegopsina. Marine and Freshwater Research 55, 341–355.


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Manuscript received 19 September 2003; revised 8 December 2003; and accepted 23 March 2004.

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