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First published online December 14, 2006
Journal of Experimental Biology 210, 1-11 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.02588
On the depth and scale of metabolic rate variation: scaling of oxygen consumption rates and enzymatic activity in the Class Cephalopoda (Mollusca)
Biological Sciences Department, University of Rhode Island, 100 Flagg Road, Kingston, RI 02881, USA
e-mail: seibel{at}uri.edu
Accepted 9 October 2006
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Summary |
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 TOP Summary IntroductionMaterials and methodsResultsDiscussionConclusionsReferences |
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Key words: metabolic scaling, citrate synthase, metabolic theory, deep-sea
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionConclusionsReferences |
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; Calder,
1984; Peters,
1983; Kleiber,
1932; Rubner,
1883; Brody and Proctor,
1932; Heusner,
1991; Hemmingsen,
1960; Zeuthen,
1953; White and Seymour,
2005). Metabolic intensity (i.e. the mass-specific rate of
metabolism, B) typically decreases with increasing body mass
(M) according to:
 | (1) |
where b0 is a normalization constant independent of mass and the
exponent, b, is a scaling coefficient that often falls near
quarter-power (b=-0.25) (Savage et al.,
2004; Farrell-Gray and
Gotelli, 2005). Quarter-power metabolic scaling is viewed by some
as a biological law (West and Brown,
2004), and many theories have been postulated to explain the
phenomenon [for review and critique (see
Glazier, 2005;
Agutter and Wheatley,
2004)].
The reported commonality of metabolic scaling patterns across habitats and
taxa (Gillooly et al., 2001;
Hemmingsen, 1960) has given
rise to a `metabolic theory of ecology' (MTE)
(Brown et al., 2004) that
strives to predict broad ecological and evolutionary trends from rates of
energy metabolism in individual organisms. The MTE is purposefully simple,
incorporating only mass and temperature, and is thus dependent, for predictive
power, on metabolic commonality [i.e. the similarity in normalization
constants, b0, and slopes, b (Eqn 1), across broad
taxonomic and functional groups of organisms]. The normalization constant
cannot be derived from first principles, but rather, must be fit empirically.
Proponents of the MTE acknowledge limited taxon-specific variation in
b0. Gillooly and colleagues
(Gillooly et al., 2001) report
only six-fold difference between the best-fit metabolic scaling relationships
for endotherms and multicellular ectotherms, and 20-fold variation between the
lowest unicells and highest mammals.
The MTE is founded on the idea that quarter-power scaling results from
universal geometric constraints on the transport of oxygen and fuel with
increasing size due to the hierarchical branching networks that characterize
many organismal transport systems (West et
al., 1997; West et al.,
1999). The assumptions of the model have been widely criticized
(Chaui-Berlinck, 2006;
Suarez et al., 2004;
Darveau et al., 2002;
Weibel and Hoppeler, 2005;
Hulbert and Else, 2005;
Porter, 2001;
Clarke, 2006;
Bokma, 2004;
Dodds et al., 2001) and
vigorously defended (Gillooly et al.,
2006; Brown et al.,
2004). Implicit in many of the criticisms is the idea that rates
of metabolism reflect organismal energy demand and that constraints on oxygen
delivery cannot adequately explain the size-dependence of basal metabolic
rate. As such, they have important implications for the MTE and the
mechanistic basis for the patterns it describes.
Different normalization constants, found between closely related species
living in different environments, different phylogenetic lines, and between
athletic and more sedentary species (Biggs,
1977; Childress and Somero,
1990; Reinhold,
1999; Weibel and Hoppeler,
2005; Reich et al.,
2006; Makarieva et al.,
2005; Seibel and Drazen, in press), are often subtle and appear as
noise in the allometric relationships observed over large mass ranges.
However, large taxon-specific differences in normalization constant would
effectively diminish the generality of the MTE, allowing ecological
predictions only for highly specific groups of organisms. Furthermore,
species-specific differences in normalization constant will influence
interspecific scaling coefficients, regardless of the root cause(s) of scaling
relationships.
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), in
eight families within a single class of organisms, the Cephalopoda.
Cephalopods are similar to the well-studied mammals in that they occupy an
adult size range, from pygmy octopuses to colossal squids, of more than six
orders of magnitude. That size range is expanded here to more than seven
orders of magnitude by inclusion of ontogenetic metabolic series, from
juveniles to adult stages. Furthermore, cephalopods have a closed circulatory
system functionally analogous to that of vertebrates and so should, of all
invertebrates, most precisely match the conditions required for quarter-power
scaling as first outlined by West and colleagues based on the vertebrate
circulatory system (West et al.,
1997). Cephalopods are found in all marine habitats, from the
poles to the tropics, and to the deep ocean trenches below at least 7000 m.
They are abundant, commercially important in some cases, and are increasingly
dominant components of marine ecosystems
(Boyle and Rodhouse, 2005).
This is the first comprehensive analysis of metabolic scaling for
cephalopods. |
Materials and methods |
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;
Seibel et al., 2000).
Temperature dependence
All oxygen consumption rates within the families Gonatidae, Cranchidae,
Histioteuthidae, Bolitaenidae and Vampyroteuthidae (132 measurements in
total), and some members of the Octopodidae and Ommastrephidae (10
measurements), were measured by the present author at 5°C
(Seibel et al., 1997;
Seibel and Childress, 2000)
(B.A.S., unpublished). All of those species experience 5°C at some point
within their daily or ontogenetic distributions. Most individuals in other
families (76 measurements in total) were standardized to 5°C assuming a
Q10 of 2.5. Temperature coefficients reported for some species were
unusually high [e.g. Q10=5.6 for Illex illecebrosus
(DeMont and O'Dor, 1981)] while most others fell near 2.5
(O'Dor and Wells, 1987).
Errors in Q10 estimation will lead to variation in both slopes and
normalization constants of the relationships observed. In the case of
normalization constants, such errors are small and could not significantly
influence the 200-fold variation observed (more than 100-fold variation is
observed just within species measured at 5°C). Scaling coefficients may be
much more sensitive to these errors, but arguments presented in the discussion
suggest that the present results are not unduly influenced by the method of
temperature correction.
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).
Furthermore, the curves for loliginid and ommastrephid squids are above the
mammalian curve across the entire size range when adjusted using any
Q10 value higher than 1.8. Only at unusually low Q10
values do the metabolic rates of squids and mammals overlap. Even if no
temperature correction is applied to mammals, some overlap between squid
(5°C) and mammalian (37°C) metabolic rates is observed.
Statistics and phylogenetic independence
Power regressions were generated using Statview 5.01 (SAS Institute, Cary,
NC, USA) and significance of all relationships is at 95% confidence level.
Differences in scaling coefficients (i.e. slopes) were assessed by Analysis of
Covariance (ANCOVA, Statview 5.01). All oxygen consumption rate data points of
a given symbol (Fig. 1)
represent individuals within a family. Some families are represented by only
one species while others are represented by several. The phylogenetic
independence of the data was previously assessed using independent contrasts
(Seibel and Carlini, 2001). An
analysis of higher nodes further demonstrated that most of the variation in
cephalopod metabolism is between families within an order, as opposed to
species or genera within a family (Seibel
and Carlini, 2001). Thus the use of families as the comparative
unit allowed greater size range in some cases while not violating assumptions
regarding phylogenetic independence of the data. The analysis of intraspecific
scaling in Fig. 2 demonstrates
a pattern similar to the familial relationships. Phylogeny does not drive the
decline in metabolism with depth (Seibel
and Carlini, 2001) (Fig.
3).
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The use of either whole-animal metabolism or mass-specific metabolism is
dependent on preference as well as the question being asked. Obviously a
larger organism has more respiring tissue and will consume more oxygen. Thus,
a whole-organism scaling curve is, to an extent, a statement of the obvious
and provides a false sense of the magnitude of variation. I opted to present
mass-specific oxygen consumption rates
(
O2; µmol O2
g-1 h-1) for this reason and because some phenomena
addressed by the MTE, for example rates of DNA base-pair substitution
(Gillooly et al., 2005),
depend on `metabolic intensity' rather than whole-organism metabolism.
Furthermore, the enzymatic data I present are an inherently mass-specific
value measured by grinding a sample of muscle tissue rather than an entire
organism. Thus for graphic comparison of the slopes, mass-specific oxygen
consumption rates were presented with mass-specific enzymatic activities.
Whole-animal metabolic rates lead to the same conclusion and can be calculated
simply by multiplying rates by the mass values listed in supplementary
material Table S2.
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).
Most of the variation in metabolism mentioned above is found between families
and is directly related to the habitat depth
(Fig. 3), which is similar for
individual species within each family
(Seibel et al., 1997;
Seibel et al., 2000). Some
variation is found between species within a family, as indicated in
Fig. 2; however, additional
data is required to determine significance of the differences in most
cases.
The variation in normalization constants (b0; Eqn 1) of
cephalopod oxygen consumption and enzymatic activity is explained largely by
habitat depth [Fig. 3;
O2,
b0=79.1MDO-0.9; r2=0.92; CS,
b0=141.2MDO-0.80, where MDO=minimum depth of occurrence;
r2=0.94; (Seibel et
al., 1997; Seibel et al.,
2000)]. Individual species within each family are found over
similar depth ranges. Normalization constants ranged from 8.2 for ommastrephid
squids to 0.14 for the bathypelagic vampire squids. This difference is further
enhanced at large sizes due to variation in scaling coefficients. Five of
eight cephalopod families analyzed had scaling coefficients (b in Eqn
1) not significantly different from a quarter power. However, each epipelagic
squid family (Gonatidae, Loliginidae and Ommastrephidae) had a shallower
scaling coefficient that, in the case of Loliginidae, was significantly
different from -0.25. Intraspecific scaling slopes are presented in
Fig. 2 and
Table 2 and most of them are
similar to those reported here for familial relationships
(Fig. 1;
Table 1)
(Glazier, 2005;
O'Dor and Wells, 1987). The
intraspecific scaling coefficients for epipelagic squids are significantly
higher (less negative) than for mesopelagic species
(Fig. 2C), a pattern consistent
with other pelagic animals (Glazier,
2006).
Metabolic rates of cephalopods are compared to a variety of animal taxa
living in diverse environments in Fig.
4. Body mass accounted for only 68% of the variation in
whole-animal metabolism (13% on a mass-specific basis) within all cephalopods
combined. If one considers that additional body mass consumes incrementally
more oxygen, a large fraction of the variation in whole-animal metabolism
should be explained by body mass. For comparison, recent analyses found that,
after temperature adjustment, mass accounts for 94% of the variation in
mammalian whole-animal basal metabolic rates
(White and Seymour, 2005).
Thus, the relatively low correlation coefficients found for combined
cephalopod metabolism signifies tremendous interspecific diversity in
metabolic rates. All data and their sources are available in supplementary
material Tables S1-S4 online.
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Discussion |
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),
Cephalopod metabolism varies between species by as much as 200-fold beyond the
effects of mass and temperature (Fig.
1). Furthermore, scaling coefficients of some species deviate
significantly from the quarter power relationship that underpins the MTE
(Gillooly et al., 2001;
Savage et al., 2004;
Brown et al., 2004;
West et al., 1997;
West et al., 1999)
(Fig. 1; Tables
1,
2). Mass, while an important
metabolic determinant within many individual species
(Fig. 2), is a relatively minor
determinant of routine metabolism among all cephalopods at a common
temperature. As described in detail below, large taxon-specific differences in
normalization constant within Cephalopod molluscs
(Fig. 1), and more broadly
(e.g. fishes), reflect important interspecific differences in energy demand as
dictated by the particular ecological niche inhabited by a species (e.g.
habitat depth and foraging mode, Fig.
3). The observed metabolic variation is not restricted to
cephalopods (Fig. 4), a fact
that calls into question the generality of metabolic scaling and the
application of scaling to macroecological theory.
Ecological basis of metabolic variation
The majority of metabolic variation observed here stems from differential
selection for muscular energy demand [i.e. locomotory capacity
(Seibel et al., 1997;
Seibel et al., 1998;
Seibel et al., 2000)].
Locomotory capacity is an important determinant of animal metabolism in any
environment, but its influence is enhanced within the expansive pelagic
biosphere by the depth-related gradient in light available for predator-prey
interactions (Childress, 1995;
Seibel and Drazen, in press). Shallow-living squids (referred to hereafter as
`epipelagic') spend at least some portion of their day in active pursuit of
prey through surface waters. In nature, such squids swim continuously by jet
propulsion at low efficiencies (O'Dor and
Webber, 1986) and have consequently evolved among the highest
temperature-corrected metabolic rates of any organisms, including
heterothermic fishes, flighted insects and mammals
(Fig. 4)
(O'Dor and Webber, 1986;
Shulman et al., 2002;
Clarke and Johnston, 1999;
Reinhold, 1999;
O'Dor and Webber, 1986).
Interestingly, metabolism in coastal loliginids is indistinguishable from the
more oceanic ommastrephids despite several published reports to the contrary
(Fig. 1A). In contrast, demand
for locomotion among deep-living (meso- and bathypelagic) sit-and-wait
predators, as indicated by physiological proxies as well as direct submersible
and shipboard observations, is greatly diminished (Seibel and Drazen, in
press; Seibel et al., 2000).
Such species swim sluggishly, but with greater efficiency than
shallower-living species (Seibel et al.,
1997; Seibel et al.,
1998; Seibel et al.,
2000).
Habitat depth and visual predator-prey interactions
The present analysis confirms that bathypelagic cephalopods have routine
metabolic rates and enzymatic activities up to 200-fold lower than their
shallow-living relatives (Fig.
1). Sizecorrected metabolism and citrate synthase activity
(normalization constants from relationships in
Fig. 1A,B;
Table 1) in cephalopods are
strongly and inversely related to the minimum habitat depth occupied by a
family (Fig. 3)
(Seibel et al., 1997;
Seibel et al., 2000). That
these depth trends are independent of mass and temperature is made clear by
the present analysis. The close correspondence between scaling relationships
for oxygen consumption rates and enzymatic activities argues strongly that
these results are not artifactual (Fig.
1; Table 1).
However, the extent to which metabolic rates decline with depth depends on the
size chosen for normalization because of the divergent scaling relationships
of deep- and shallow-living species.
Strong depth-related trends in metabolism and enzymatic activity have been
reported only for visually orienting pelagic predators, such as fishes,
crustaceans and cephalopods (Childress,
1995; Seibel et al.,
1997; Torres and Somero,
1988). More than 30 years of careful comparative study
demonstrates these trends to be independent of surface productivity (a proxy
for food availability), oxygen content and phylogeny (for reviews, see
Childress and Seibel, 1998;
Childress, 1995;
Thuesen et al., 1998;
Seibel and Carlini, 2001;
Seibel and Drazen, in press). The decline in metabolism with depth is
explained, not by environmental constraint at depth, but by strong selection
for high locomotory capacity in well-lit surface waters and a relaxation of
that selection with light-limitation at depth [i.e. the `visual interactions
hypothesis' (Childress, 1995;
Seibel and Drazen, in press)].
Visible light decreases linearly with depth and is absent below 1000 m.
According to the `visual interactions hypothesis', the distances over which
visually orienting predators and prey detect each other, and the distances
they must swim to catch or avoid one another, are substantially reduced in the
deep pelagic biome. Consequently, the requirement for high metabolic rates
and, as indicated by mitochondrial enzyme activity in locomotory muscles,
locomotory capacity, is similarly reduced
(Fig. 1B)
(Seibel et al., 2000). The
depth-related decline is especially pronounced in cephalopods due to the
differences in locomotory efficiency and buoyancy between deep- and
shallow-living species (Seibel et al.,
1997; Seibel et al.,
2000; Seibel et al.,
2004) and to the divergent scaling relationships demonstrated
here. Reduced demand for locomotion is generally accompanied by reduced
protein, increased water and lower mitochondrial abundance in locomotory
muscles, all of which contribute to reduced resting or routine metabolic rates
(Childress, 1995;
Seibel et al., 2004).
The visual interactions hypothesis is supported by the lack of
depth-related trends in metabolism for non-visual pelagic taxa [e.g. medusae,
chaetognaths or copepods (Thuesen and
Childress, 1994; Thuesen and
Childress, 1994; Thuesen et
al., 1998)], and in benthic visual taxa that have greater
opportunities for crypsis and refuge from predation
(Childress et al., 1990;
Seibel and Childress, 2000).
All species within each of the pelagic cephalopod families analyzed here are
found at similar depths (e.g. all loliginids are shallow-living while all
bolitaenids are deep-living) but this is not true of the benthic Octopodidae.
However, benthic octopods, as well as other benthic groups, appear to have
temperature-corrected metabolic rates that do not vary significantly with
habitat depth (Fig. 1A). The
similarity in metabolic rates within benthic groups of organisms is a
reflection of the similarity of lifestyles among benthic species
(Childress, 1995;
Seibel and Childress, 2000;
Seibel and Drazen, in press). While benthic animals can burrow in the sediment
and hide in crevices to avoid detection by predators, pelagic species lack
such refuge.
Metabolic state and the meaning of enzymatic activities
Implicit in the visual interactions hypothesis is the idea that the
measured routine or resting metabolic rates reflect the metabolic and
locomotory demands on these animals in nature. Such `field' metabolic rates
are obviously intermediate between resting and maximum rates of metabolism
(O'Dor, 2002;
O'Dor et al., 1994). Studies
have documented a close relationship, despite divergent scaling relationships
in some cases (Weibel and Hoppeler,
2005), between resting and maximum aerobic metabolic rate
(Reinhold, 1999). The nature
of this linkage is not fully understood but may relate to added maintenance
costs for machinery that supports elevated locomotory activity as well as
evolutionary trade-offs between resting costs and scope for activity
(Clarke, 2006;
Reinhold, 1999; Seibel and
Drazen, in press).
Citrate synthase activities typically correlate with the metabolic capacity
required for sustained exercise [e.g. active or maximum, rather than resting,
metabolic rates (Moyes, 2003;
Weibel and Hoppeler, 2005)].
However, at least in a broad interspecific comparison, such as that presented
here, a correlation between enzymatic activity and routine rates is not
surprising and reflects divergent locomotory capacity between deep- and
shallow-living species as discussed above. The apparent correlation between
scaling coefficients for enzymatic activity and routine oxygen consumption
rate are intriguing and require further study. Scaling of maximum metabolic
rate has not been addressed systematically in cephalopods but the few
available data suggest a positive mass-specific scaling coefficient. Smaller
species of loliginid squids appear to have limited aerobic scope compared to
larger species (e.g. Bartol et al.,
2001; Webber and O'Dor,
1986; Finke et al.,
1996).
Scaling coefficients
The present data do not support the existence of a universal scaling
coefficient (Table 1). Three of
eight families have scaling coefficients significantly different from quarter
power. The shallower slopes all belong to families of epipelagic squids and
are consistent with the few intraspecific literature values available
(Table 2;
Fig. 2B). A significant
difference was found between intraspecific scaling coefficients of epipelagic
and mesopelagic cephalopods (Fig.
2C). O'Dor and colleagues
(DeMont and O'Dor, 1984;
Webber and O'Dor, 1986;
O'Dor and Wells, 1987)
controlled activity and body size independently in Illex illecebrosus
and found that mass-specific metabolism was not dependent on body mass, at
least over the limited size range available. Similar results have been
reported previously for ommastrephid
(Zuyev et al., 2002),
onychoteuthid (reviewed in O'Dor and
Wells, 1987) and loliginid
(Segawa, 1995;
Segawa and Hanlon, 1988;
Wells et al., 1988) squids. A
few studies report an intraspecific exponent near quarter-power for epipelagic
squid species (Table 2)
(Segawa, 1991;
Bartol et al., 2001) but
conflicting studies exists for the same species. Combining studies to enhance
the intraspecific size range reveals a shallow scaling coefficient for
Loligo forbesi (b=-0.09; Loliginidae;
Table 2) and preliminary data
suggest a shallow slope for Dosidicus gigas over six orders of
magnitude size range (b=-0.06,
Table 2).
Interestingly, the intra- and interspecific scaling relationship within the
Octopodidae varied. While the present interspecific study demonstrates scaling
near a quarter-power for benthic octopods, three independent studies report
relatively shallow intraspecific scaling coefficients for this group
(Maginnis and Wells, 1969;
Segawa and Hanlon, 1988;
Katsanevakis et al., 2005).
Only one intraspecific study (Wells et
al., 1983) showed quarter-power scaling
(Fig. 2A;
Table 2). Obviously the
relationship between intra- and interspecific metabolic scaling remains an
open and intriguing question that hinges on the trade-off between required
size range, sample size, and the similarity of normalization constants
(b0) and slopes (b) for the species included (see
Table 2). The slope of an
interspecific relationship may be significantly altered by species-specific
differences in scaling parameters. Thus, the method used must depend on the
precision required for the question between addressed.
While maximum metabolic rates in mammals
(Weibel and Hoppeler, 2005)
scale with a shallow slope similar to that reported here for epipelagic
squids, it is important to point out that the present squid data do not
reflect high levels of activity during measurement. The rates presented here
are termed `routine' because spontaneous activity within the respirometry
chambers was not controlled in most cases, but all rates were measured
under conditions that minimized activity levels to the extent possible.
For example, measurements for which activity was not specifically controlled
were performed on animals that were acclimated for several hours,
post-absorptive, and held in darkened respirometry chambers. Maximum, active
or field metabolic rates have only been measured for some species in the
families Loliginidae and Ommastrephidae
(O'Dor, 2002) and they are
substantially higher than the rates used in the present analysis.
Shallow scaling relationships are also not an artifact of temperature
correction. All rates presented here were measured at 5°C with the
exception of those in the families Loliginidae, Ommastrephidae and some
benthic Octopodidae. Metabolism in those families was adjusted to 5°C,
assuming a Q10 of 2.5. While published Q10 values for
cephalopods vary widely, most fall near this value
(O'Dor and Wells, 1987).
Sufficient data exists for the family Loliginidae and Ommastrephidae,
combined, to analyze scaling at a common measurement temperature of
13±1°C. That analysis also revealed a shallow slope over a mass
range of more than six orders of magnitude (b=-0.15, N=8).
Furthermore, as stated above, published mass-specific metabolic scaling
coefficients for loliginid and ommastrephid squids are generally greater (less
negative) than -0.25 (Fig.
2B,C; Table 2).
Lastly, the close correspondence between enzymatic activities (all measured at
20°C) and oxygen consumption rates (measured or adjusted to 5°C), in
both b0 and b, provides assurance that the errors in
temperature correction are not substantially influencing the observed
relationships (Fig. 1).
Despite the tremendous numbers of variables that could work synergistically
to cause the observed scaling relationship for any given species
(Suarez et al., 2004),
hypotheses put forward to explain the phenomenon of metabolic scaling
generally fall into only a few categories (see
Glazier, 2005;
Agutter and Wheatley, 2004).
Most hypotheses reflect the slower rate of increase of effective surface area
or cross section of a solid as its mass increases
(Childress and Somero, 1990).
Many hypotheses, including the recent contribution upon which the MTE is
founded (e.g. West et al.,
1997; West et al.,
1999; Banavar et al.,
1999), suggest that geometric scaling rules impose constraints on
the design of animals such that some surface (be it internal or
external)-limited supply or removal processes (e.g. gas exchange or digestion)
increases more slowly than does mass and that metabolism necessarily follows.
Alternatively, Childress and Somero argue
(Childress and Somero, 1990)
that the usual negative allometry of basal aerobic metabolism is due to
increased (geometric) opportunities for energy savings in larger animals as a
result of reduced costs at large sizes for such processes as thermoregulation
in mammals, ion regulation in fishes
(Childress and Somero, 1990),
or cost of transport in mobile species
(Suarez et al., 2004;
Glazier, 2006). Cephalopods
shed unique light on this ongoing debate but ultimately provide no resolution
because several plausible, non-exclusive, hypotheses can be formulated that
explain, equally well, the near-isometric metabolic scaling observed in
epipelagic squids.
Cutaneous respiration and exchange surfaces
Despite remarkable ecological and physiological convergence with marine
vertebrates (Seibel and Drazen, in press;
O'Dor and Webber, 1986),
epipelagic squids exhibit a few key differences in form and function that, in
combination, may alleviate the hypothesized constraints or deny squids the
hypothesized opportunities for energy savings associated with the scaling of
exchange surfaces. The oxygen-carrying capacity of the cephalopod circulatory
system is limited, relative to vertebrates of similar aerobic capacity,
requiring that they make maximal use of all blood-borne oxygen, even at rest
(Pörtner, 2002;
Finke et al., 1996). However,
carbon dioxide production is in excess of the oxygen capacity of the blood
suggesting that they acquire additional oxygen, as much as 60% of demand,
across the skin (Pörtner,
2002). Diffusion distances typically increase with animal size,
presumably diminishing the utility of cutaneous oxygen uptake in large
animals. However, the body of epipelagic squids is effectively a hollow tube,
with internal and external surfaces inherently well suited for cutaneous
oxygen uptake. As such squids grow, their mantle diameter increases faster
than thickness. As a result, total surface area relative to volume
(SA1/2:V1/3) actually increases with
size (O'Dor and Hoar, 2000).
Blood vessel density is relatively low throughout the mantle while
mitochondria are most abundant along the internal and external surfaces
(Bone et al., 1981;
Mommsen et al., 1981), an
arrangement that maximizes the PO2 gradient across the
skin and ensures maximal use of diffused oxygen.
Thus, if exchange surfaces are critical determinants of metabolic scaling,
metabolism in epipelagic (tube-shaped) squids are expected to diverge from
other cephalopod groups with increasing size. In support of this hypothesis I
show that scaling of mass-specific metabolism and citrate synthase activity in
epipelagic squids (Loliginidae, Ommastrephidae and Gonatidae) approaches
mass-independence (b<-0.10) while metabolism in other cephalopod
groups scales near a quarter-power (Fig.
2C). Other cephalopods are also dependent to varying extents on
cutaneous respiration [e.g. Octopus vulgaris
(Madan and Wells, 1996)].
However, the ratio of surface to volume does not increase with size in other
species (i.e. SA1/2:V1/3 is constant
across the size range). The comparison between squids and octopods should be
viewed with some caution because, although the present analysis shows
quarter-power scaling in the benthic family Octopodidae, three (of four)
intraspecific metabolic scaling studies for this group found shallow scaling
coefficients, similar to the epipelagic squids as discussed above
(Fig. 2A). The near-isometric
metabolic scaling in some pelagic taxa [e.g. ctenophores and salps
(Glazier, 2005;
Glazier, 2006)] may reflect,
as I have suggested above for squids, near isometric scaling of surface to
volume ratios in conjunction with reliance on cutaneous respiration (cf.
Thuesen et al., 2005).
Cost of transport
One recent hypothesis suggests that size-related increases in the energy
costs of swimming or of rapid rates of growth and reproduction in response to
high levels of mortality (predation) in open water may lead to scaling
coefficients that approach isometry in epipelagic animals
(Glazier, 2005;
Glazier, 2006). Glazier notes
several phyla of pelagic animals within which metabolism scales isometrically,
while quarter-power scaling is more common in benthic species of these same
phyla (Glazier, 2006). Four
families of pelagic cephalopods examined here scale near quarter-power, but
all are deep-living and presumably experience lower levels of predation. In
support of Glazier's hypothesis, the fast-growing, high capacity species scale
nearly isometrically. Benthic octopods, with an exponent near quarter-power,
also appear to support Glazier's argument (but as noted above, the
intraspecific scaling coefficients differ). However, many other pelagic taxa
scale near quarter-power suggesting that other factors must also be at work
(e.g. Seibel and Dierssen,
2003; Thuesen and Childress,
1994) [but for comprehensive survey, see Glazier
(Glazier, 2005)].
Several authors have postulated a relationship between metabolic scaling
and locomotory costs. Stride or fin stroke frequency is directly proportional
to power output or metabolic cost, and necessarily declines with size
(Suarez, 1996;
Suarez et al., 2004;
Glazier, 2005;
Seibel et al., 1998;
Schmidt-Nielsen, 1984;
Bejan and Marden, 2006). The
observed scaling patterns may, thus, reflect the cost-of-transport (COT),
which decreases rapidly with size in mammals, birds and fishes
(Suarez et al., 2004;
Childress and Somero, 1990),
but not in epipelagic squids. Limited data suggests that cost of transport
scales differently for jet propulsion (M-0.2) and fin
swimming (M-0.3), such that jetting is more efficient than
fin swimming at small, but not large, sizes
(O'Dor and Webber, 1986;
Seibel et al., 1998;
Thompson and Kier, 2001). The
divergent scaling coefficients for epipelagic squids and fishes suggest that
COT may play a role in metabolic scaling.
|
Conclusions |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionConclusionsReferences |
|---|
;
Reinhold, 1999; Seibel and
Drazen, in press). To put the metabolic variation in perspective, a
deep-living vampire squid (Vampyroteuthis infernalis) weighing just 1
g has the same mass-specific metabolic rate as an elephant
(
106 g; extrapolation of the curve in
Fig. 3) while an epipelagic
squid weighing 10 kg has the same mass-specific metabolic rate as a mouse
(10 g; Fig. 3). Only brief
behavioral observations are required to demonstrate qualitatively that deep-
and shallow-living pelagic cephalopod species have a vastly different mode and
pace of life despite overlapping body mass and temperature ranges.
Nevertheless, proponents of the MTE (Brown
et al., 2004; Gillooly et al.,
2001) have overstated the influence of body size and temperature
on metabolic rate to the exclusion of such obvious differences in lifestyle,
ecology and evolution.
The limited survey of available metabolic data from which reports of
metabolic commonality are derived and on which the MTE is founded, certainly
contributes to a lack of appreciation for ecological influences. For example,
the invertebrate data cited by Gillooly et al. include only 25 measurements of
15 species (Gillooly et al.,
2001). While they represent diverse phyla, all included species
have similar lifestyles that involve crawling on, or burrowing in, the ground
or sediment. There are no flying, swimming or floating representatives. It is
therefore not too surprising that the data approximate a single scaling
relationship once corrected for temperature differences. Seibel and Drazen
found that the variation in normalization constants between benthic groups
within a phylum is not nearly as pronounced as that for pelagic groups in
those same phyla (Seibel and Drazen, in press). There is, of course,
substantial variation within and between groups of benthic organisms, but
normalization constants of benthic groups cluster more closely than do pelagic
groups reflecting a more limited range of activity levels on the benthos
regardless of depth (Fig. 4)
(Seibel and Childress,
2000).
The diversity of metabolic rates within the Cephalopoda should not be
viewed as exceptional. The pelagic biosphere is the largest ecosystem on the
planet (Robison, 2004) and the
metabolic rates of its inhabitants, both invertebrates and vertebrates, cannot
be adequately described, nor even approximated, by a single allometric
relationship that incorporates only mass and temperature (Figs
1,
2). For example, the
ecologically important and abundant cnidarians and ctenophores push the
envelope with the bathypelagic cephalopods at the lower, while the tunas,
epipelagic sharks and flighted insects join epipelagic squids at the upper,
end of the metabolic spectrum (Fig.
4). Substantial variation in normalization constants has been
reported within fishes, crustaceans, annelids, mollusks
(Fig. 4) (Seibel and Drazen, in
press), mammals (Weibel and Hoppeler,
2005), insects (Reinhold,
1999), plants (Reich et al.,
2006) and unicells (Makareiva et al., 2005). Wide variation in
intra- and interspecific scaling coefficients (b; Eqn 1) has also
been reported (Glazier, 2005;
Glazier, 2006).
Thus, I suggest that mass, while an important metabolic determinant within appropriately constrained phylogenetic or functional groups, is not an especially useful predictor of metabolism within such broad groups of organisms as `invertebrates', `vertebrates' or `ectotherms'. Moreover, there is no valid reason for separating vertebrates from invertebrates or ectotherms from endotherms in metabolic rate models, given that all fish and mammalian rates fall within the range of invertebrate data (Fig. 4). The appropriate taxonomic level of analysis depends on the question being asked and thus, the precision with which metabolic rates must be modeled. An ecological model that requires independent determination of scaling coefficients and normalization constants for each species is of limited value. My analysis reveals the predictive limitation of the MTE by demonstrating that metabolic scaling relationships (and their hypothesized mechanistic basis) are not universal and that mass is not the primary determinant of metabolic intensity. The divergent lifestyles of deep- and shallow-living pelagic cephalopods provide an ecological `signal' for metabolism that clearly emerges from the allometric `noise' and demonstrates a dominant role of ecology in determining metabolic rates.
|
Acknowledgments |
|---|
|
Footnotes |
|---|
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