4 General Discussion
4.3 Growth efficiency and productivity
Viewed in the light of the previous chapter low rates of standard metabolism in cold- stenothermal organisms is a positive energy advantage, as they lead to increased ecological growth efficiency because of lower maintenance costs (Clarke 1987, Clarke and Crame 1989).
Proxy for growth efficiency
Polar marine invertebrates tend to grow slowly (Brey and Clarke 1993, Arntz et al.
1994, Peck 2002) and historically this has been explained either as a direct rate-
limitation by temperature or by an elevated metabolic rate, as suggested by t h e
2 4 6 8 10 12
Temperature (¡C
Figure 4.7 Relationship of the ratio between standard metabolic rate (SMRAvg) and overall growth performance (P) to arnbient temperature of 7 scallop species (grey dots:
A. opercularis, C. islandica, M. varia, M, yessoensis, P.
magellanicus, Z. patagonica; black dot: A. colbecki). Data presented are resting or standard metabolic rates at normal ambient temperatures. Where seasonal data were available the data were averaged over the whole year (for more details and references See publication II, p 77).
The ratio of OGP-to-SMRAvg was established as a proxy for growth efficiency. I.e., it is presumed to be proportional to the fraction of metabolic energy channelled into somatic growth. Good evidence has been produced in ternperate bivalve molluscs, e.g. Mytilus edulis, that individuals with low basal or standard metabolic requirements show comparatively higher growth rates (for details Hawkins et al. 1989, Wieser 1994, Hawkins and Day 1996) and thus OGP-to-SMR ratios would be relatively high, too.
The general decrease of growth efficiency with temperature, as shown in Figure 4.7, gives evidence that metabolic rates increase faster with temperature than does growth performance, possibly as a consequence of enhanced maintenance cost or cost of growth or both. The temperature coefficients (Qio) computed from the corresponding Arrhenius rnodels exemplify this difference: within the 0-25'C temperature range Qlo of scallop metabolic rate is 2.28 (publication IV, pp 94) whereas overall growth performance changes more slowly with temperature (Qlo=
1.12, publication IV, pp 95).
In conclusion, irrespective at which hierarchical level limitations and constraints are initiated, studies within single species led to the hypothesis that the primary
physiological basis of an increase in production is reduced energy expenditure per unit of growth, indicating enhancements of growth efficiency, rather than a straightforward increase in feeding and all other associated processes that are required for growth (Diehl et al. 1986, Hawkins et al. 1986, 1989, Hawkins & Day 1996).
Production and productivity
All energy acquired by animals through the ingestion of food is ultimately either used in metabolic processes, or deposited as new body tissue (growth or reproduction). The partitioning of ingested or metabolizable energy into maintenance and production and possible trade-offs between growth and production are important to characterize species-specific life histories (e.g. Sibly and Calow 1986, Wieser 1994). The changing patterns of individual energy expenditure during the lifetime of the three investigated species are discussed in detail in the respective chapters (A.
opercularis: publication V, pp 97-112; A. colbecki: publication I, pp 51-64; Z.
patagonica: chapter 3.3). These energy budgets clearly illustrate some general age- related patterns: (i) an increasing share of maintenance requirements (expressed as respiration) with age, and (ii) a progressive transition of production from somatic growth to gonad output with age, as previously observed in other scallop species, too e . g . Shafee 1982, Fuji and Hashizume 1974, MacDonald and Thompson 1985, 1988, Claereboudt and Himmelman 1996). The general decrease of somatic growth with increasing age (Calow 1977), however, is not necessarily caused only by a shift between PS and Pg or the declining ability of the older animals to convert assimilated food into new tissue (Calow and Townsend, 1981), but may also be caused by a shorter growing season of older individuals, as already shown for Chlamys islandica (Vahl 1981) and Pecten maximus (Chauvaud and Strand 1999). To define the crucial factor within the investigated populations derives further investigation and a narrow sampling frequency.
Net (Kz) and gross growth efficiency (K,) and turnover ratio (PIB) indicate to which extent energy translates into production available for the next trophic levels. In Tab.
4.4 values for several pectinid populations are summarized. Calculations of population production indicate that populations of short-lived scallop species such as A. opercularis and Mimachlamys varia invest around 15% of the total annual production into reproduction (Tab 4.4). In populations of iong-lived species this proportion is distinctly higher: Placopecten magellanicus (MacDonald and Thompson 1985) and Patinopecten caurinus (MacDonald and Bourne 1987) channel more than 50% of their annual production into gametes, whereas the cold-water species
Chlamys islandica and Adamussium colbecki invest approximately 20-30% (Vahl 1981a, b, publication I, pp 51-64).
Table 4.4 Energy effiencies of various scallop populations
Speciesl Place "Ki 'KK, "Ps 'PIB Reference [kJ m-2
Adamussium colbecki Antarctica 0.05
Aequipecfen opercularis
France 0.16
Chlamys islandica
Norway 0.08 Mimachlamys varia
France France
Mizuhopecten yessoensis
Japan 0.32
Pafinopecfen caurinus Canada
Placopecfen magellanicus Canada
Canada
Zygochlamys patagonica Argentina 0.05
Chiantore et al. 1997;
publication l publication V Vahl 1981 Shafee & Conan 1984 Shafee & Conan 1984
Fuji & Hashizume 1974
MacDonald & Bourne 1987
MacDonald & Thompson 1985, 1986,1988
This study gross growth efficiency, K,= P-rot/C; net growth efficiency, K2= P-roi/A; somatic production;
'
gonad production; turnover-ratio
Metabolie costs of reproduction
Based on the seasonal measurements of metabolism of mature and immature A.
opercularis (publication V, pp 97-1 12) and A. colbecki (publication II, pp 65-80) specimens it is possible to estimate the metabolic costs of reproduction. Figure 4.8 compares the share of growth, basal metabolism and reproduction in individual total energy expenditure of the two species: While the proportion of basal metabolism is similar, the Antarctic scallop invests a higher proportion into growth and correspondingly less into reproduction. These data are crude estimates only, but nevertheless, provide a good base for some general annotations. In the two-species comparison of this study there is no evidence of a proportionally lower basal metabolism as previously hypothesised by Clarke (1983, 1987) for Antarctic
invertebrates. Differences in the proportion used for growth and reproduction can be explained in two ways: (i) Life strategy: The long-lived Antarctic scallop, A. colbecki,
BOX 4.1 Calculation of metabolic costs A physiological approach of the traditional en
into consideration the respiratory costs of synthesis. The major difficulty is to separate measured metabolic rates into reproductive and non-reproductive components as the mostly occur at the Same time The following estimates are based on the assumption that basal metabolic rates do not change with season,
(i) A. colbecki
Costs (reproduction) = SMR,nd(summer-mature)
-
SMRlnd(summer-immature) Costs (growth) = SMRind(summer-immature)-
SMRind(winter-mature) (ii) A. opercularisMetabolie costs of reproduction were estimated as the difference between the predicted seasonal increase of oxygen consumption of immature and obsewed consumption in summer
may be Seen as a typical A-selected animal while A. opercularis may be Seen as a r- selective species. On the other hand we do not know much about reproduction of A.
A. colbecki A. opercularis
Figure 4.8 Scheme showing an estimated energy budget of A. colbecki and A. opercularis with the three main components: growth, basal metabolism and reproduction. Ratios are calculated from differences between winter and Summer, respectively, mature and immature animals (for theoretica! background and calculation details See Box 4.1).
c o l b e c k i (Berkman 1991, Chiantore et al. 2001).
If gametogenesis requires more than one Summer period, as already reported for other polar organisms e . g . S e r o l i s p o l i t a , L u x m o o r e 1 9 8 2 a n d caridean shrimps, Gorny et al, 1992) it would be more appropriate to compare lifetime budgets. (ii) Physical f a c f o r s : The cost of shell g r o w t h m a y i n c r e a s e distinctly with decreasing temperature, owing to an increase of the solubility product of CaCOs with decreasing temperature. Hence, shell production is more expansive in polar waters, so that the Antarctic scallop has to invest a relatively higher proportion into shell growth.
Summary
S M R A ~ ~ - ~ O - O G P is an inverse proxy for growth efficiency. Thus, there is strong empirical evidence that elevated temperature constrains growth efficiency in scallops and that evolutionary adaptation does not fully compensate for this effect.
Total annual gonad production of A. colbecki is twice as high as in A . opercularis,
The proportion of metabolised energy A. colbecki invest into growth is four times higher than that of A. opercularis, most likely caused by higher costs of shell production.
The long-lived Antarctic scallop, A. colbecki, is Seen as a typical A-selected animal, while A. opercularis may be Seen as a r-selected species.