Download Metabolic temperature compensation and

880
Metabolic temperature compensation and coevolution of
locomotory performance in pteropod molluscs
Brad A. Seibel,1,* Agnieszka Dymowska,*,† and Joshua Rosenthal‡
*Department of Biological Sciences, University of Rhode Island, Biological Sciences Center, 100 Flagg Road, Kingston,
RI 02881, USA; †Department of Molecular Biosciences, University of Oslo, PO Box 1041, N-0316 Oslo, Norway;
‡
Institute of Neurobiology, University of Puerto Rico-Medical Sciences Campus, 201 Blvd. del Valle, San Juan, PR 00901,
Puerto Rico
Synopsis Gymnosomatous pteropods are highly specialized planktonic predators that feed exclusively on their
thecosomatous relatives. Feeding behavior and the morphology of gymnosome feeding structures are diverse and have
evolved in concert with the size, shape, and consistency of the thecosome shell. Here, we show that the metabolic capacity
and locomotory behaviors of gymnosomes are similarly diverse and vary with those of their prey. Both gymnosomes and
thecosomes range from gelatinous sit-and-wait forms to active predators with high-performance locomotory muscles.
We find more than 10-fold variation in size-adjusted and temperature-adjusted metabolic rates within both the
Gymnosomata and Thecosomata and a strong correlation between the metabolic rates of predators and of prey.
Furthermore, these characteristics are strongly influenced by environmental parameters and predator and prey converge
upon similar physiological capacities under similar selection. For example, compensation of locomotory capacity in cold
waters leads to elevated metabolic rates in polar species. This highly coevolved system is discussed in terms of a predator–
prey ‘‘arms race’’ and the impending loss of both predator and prey as elevated atmospheric carbon dioxide levels
threaten to dissolve prey shells via oceanic acidification.
Introduction
The Pteropoda is a recently resurrected taxonomic
designation meaning ‘‘wing-foot’’ (Massy 1920, 1932;
Klussmann-Kolb and Dinapoli 2006). It includes
pelagic snails of the closely related Gymnosomata
and Thecosomata (Class Gastropoda: Mollusca).
Both groups swim by flapping their parapodia
(i.e., wings) to generate thrust, a behavior that
has earned them the common name ‘‘sea angels.’’
The Thecosomata have shells that are calcified to
varying extents and feed by extending a mucous web
into the water column to trap food (Gilmer 1972;
Gilmer and Harbison 1986). The Gymnosomata
lack shells as adults and prey exclusively on
thecosomes (Lalli 1970). In the most thoroughly
studied example, Clione limacina feeds exclusively on
Limacina helicina (Conover and Lalli 1972). The two
species grow in concert throughout their life cycles,
and sizes of predator and prey are correlated
regionally (Lalli and Gilmer 1989). The coevolution
of the gymnosome–thecosome clade has lead to the
development of highly specialized mechanisms of
prey-capture and predator-evasion in what appears
to be a predator–prey arms race (a reciprocal
relationship by virtue of its specificity) (Brodie and
Brodie 1999). Predation involves tactile recognition
of the prey species, its rapid capture using highly
specialized buccal cones (equipped with cephalopodlike suckers in some cases), and complete extraction
of the prey from its shell, using numerous hooks and
a toothed radula. Highly efficient digestion and
assimilation follow extraction (Conover and Lalli
1972, 1974; Lalli and Gilmer 1989).
Included among C. limacina’s impressive arsenal
is a multi-geared swimming system that allows
modulation between routine swimming at wingbeat frequencies of 1–2 Hz and higher speeds
involved in predator–prey interactions (Satterlie
and Spencer 1985). Locomotion is a quantifiable
component of predator–prey interactions that
has been described for several pteropod species
(Morton 1954, 1958; Lalli and Gilmer 1989;
Davenport and Bebbington 1990; Childress and
Dudley 2004; Borrell et al. 2005). The underlying
physiology, however, is well known only for
C. limacina (Arshavsky et al. 1985a, 1985b; Satterlie
From the symposium ‘‘Integrative Biology of Pelagic Invertebrates’’ presented at the annual meeting of the Society for Integrative and
Comparative Biology, January 3–7, 2007, at Phoenix, Arizona.
1
E-mail: [email protected]
Integrative and Comparative Biology, volume 47, number 6, pp. 880–891
doi:10.1093/icb/icm089
Advanced Access publication September 18, 2007
ß The Author 2007. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. All rights reserved.
For permissions please email: [email protected].
881
Metabolic rates of pteropod molluscs
and Spencer 1985; Satterlie et al. 1985, 1990). During
vertical ascent or station-holding, C. limacina swims
continuously by sweeping its parapodia through
an arc of approximately 1808 (Borrell et al. 2005).
During slow swimming, only small motoneurons
that innervate slow-twitch (‘‘red’’) muscle fibers in
the parapodia are active (Satterlie et al. 1990). Two
large motoneurons (general excitors) and fast-twitch
(‘‘white’’) muscle fibers are recruited into activity
by serotonin during episodes of fast swimming
(Arshavsky et al. 1985a, 1985b; Satterlie 1993).
Ascent velocity is correlated with wing-beat frequency even over the small range of 1–2 Hz (Borrell
et al. 2005).
A southern-ocean Clione species has been variously described as a variety, form or subspecies of
the northern C. limacina (Massy 1920; van der
Spoel 1976, 1999). Recently, Gilmer and Lalli (1990)
supported the separation of these two as independent
species based on subtle morphological differences.
For convenience, we adopt this position and refer to
the southern congener as Clione antarctica. Gilmer
and Lalli (1990) noted that the behavior of
C. limacina and C. antarctica is nearly identical,
with similar routine wing-beat frequencies at their
respective habitat temperatures, and both feed
exclusively on regional forms of Limacina helicina.
However, they noted the lack of a distinct escape
swimming response in the southern species.
Borrell et al. (2005) corroborated this important
difference.
Clione antarctica in the Ross Sea, Antarctica, lives
permanently at temperatures near 1.88C, while the
C. limacina populations we sampled routinely
experience temperatures ranging from 58C to
15.08C. Low temperatures, such as those experienced
by C. antarctica, typically depress production of
mitochondrial ATP (Clarke 1980, 1983) and may
influence output of muscle power as well (Rome
1984, 1990). In muscles doing repetitive work, the
rate of ATP hydrolysis is directly proportional to
frequency of contraction, all else being equal (Suarez
2003). Thus, in the absence of compensation, low
temperature will limit the energy and power available
for locomotion and the frequency of wing beating
must decrease with a consequent reduction in
swimming velocity.
The average consequences to fitness of failed
foraging bouts that might result from such depression in temperature are probably much more severe
for Clione spp. than for more generalist predators
(Brodie and Brodie 1999). Thus, we expect
strong selection for the maintenance of locomotory
capacity in the face of thermal constraints on
the generation of ATP. Connover and Lalli (1972)
found that the rates of capture of prey are
temperature dependent and increase up to 178C.
In preliminary investigations, we found that feeding
rates in the two congeners are similar at
their respective habitat temperatures, but higher in
C. antarctica than in C. limacina at similar
temperatures (Seibel, unpublished data), supporting
the idea that some compensation of ability to
capture prey occurs at polar temperatures.
Crockett and Sidell (1990) defined temperature
compensation as the process permitting an organism
living at low temperatures to attain greater active
metabolic rates than an organism of similar ecotype
from a warmer habitat acclimated to the same
low temperature. The continuous locomotory activity
in clionid pteropods is in stark contrast to the
sedentary lifestyle of Antarctic notothenioid fishes
that have been the basis for most metabolic studies
of temperature compensation to date (see Clarke
1983; Eastman 1994 for reviews and Kawall et al.
2002 for a recent example). Active metabolism is
not well constrained in pteropods, but is thought to
be a substantial fraction of the total energy budget
(Davenport and Trueman 1985). Thus, we expect
temperature compensation of locomotion to be
reflected in oxygen consumption by the whole
animal, as well as at the neuromuscular and
biochemical levels. Here, we take an integrative
approach analyzing locomotory behavior and correlated metabolic expenditure in a new model system
involving gymnosomes and their exclusive prey,
the Thecosomata, each with divergent lifestyles and
living in extremes of thermal environments.
Materials and methods
Collection and maintenance of specimens
Pteropods were collected in several locations and
by many different methods. Specimens from
Antarctica (C. antarctica and Limacina helicina
antarctica) and from Newfoundland (C. limacina
and L. helicina) were collected using a ‘‘jelly dipper’’
(small beaker attached to the end of a broom handle)
at locations around Ross Island (Seibel and
Dierssen 2003) and the Ocean Sciences Center in
St Johns, respectively. A smaller number of specimens were collected using a plankton net towed
through a hole drilled in the sea-ice near McMurdo
Station, Antarctica. Specimens were transported to
McMurdo Station and maintained at low densities
in small plastic containers in filtered seawater in
temperature-controlled environmental chambers
until measurement (548 h later). Other species were
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B. A. Seibel et al.
Table 1 Oxygen consumption rates (MO2, mmol O2 g wet mass1 h1) by pteropods
Species
T8C
n
Wet Mass (mg)
MO2 ( SE)
Region
2
22
2.4–14.9
5.51 (0.44)
Antarctica 1999
2
12
1.5–15.0
3.79 (0.16)
Antarctica 2001 (starved)
5
10
1.0–5.4
6.37 (0.868)
Monterey, CA
18
3
13–88
Thecosomata
Limacina helicina
Limacina helicina
Cavolinia tridentata
Corolla spp.
10.99 (3.23)
Gulf of California
24
2
6, 11
17.25, 17.23
Atlantic Florida
5
4
1100–21510
0.226 (0.11)
Monterey, CA
18
1
0.327
0.582
Gulf of California
2
31
18.8–262
2.04 (0.116)
Antarctica 2001
2
30
10.0–130
0.99 (0.050)
Antarctica 2002 (starved)
2
20
10.6–237
2.83 (0.177)
Antarctica 2001
5
23
26.0–951
1.36 (0.155)
Newfoundland
Gymnosomata
Clione antarctica
Clione limacina
Pneumodermopsis spp.
Cliopsis krohni
Thliptodon spp.
Notobranchia grandis
5
9
156–278
1.01 (0.090)
Newfoundland (starved)
10
20
55.0–632
1.95 (0.149)
Newfoundland
18
2
2.05, 3.99
Gulf of California
24
2
5
3
5
4
126–386
5, 18
40.94, 23.36
Atlantic Florida
601–938
0.060 (0.020)
Pt. Conception, CA
550–3000
0.055 (0.014)
Monterey, CA
24
1
132
1.672
Gulf of California
5
1
740
0.067
Monterey, CA (deep)
20
1
56
0.693
Gulf of California
5
1
910
0.100
Monterey (deep)
collected by hand during blue-water SCUBA
dives (Haddock and Heine 2005) near Mote
Marine Laboratory (Florida), Monterey Canyon
(California), or in the Gulf of California (Mexico).
Notobranchea grandis and Thliptodon spp. were
collected using detritus or suction samplers on the
remotely operated vehicle (ROV) Tiburon from
the Western Flyer, Monterey Bay Aquarium
Research Institute (Robison 1993). Specimens
were allowed at least 24 h to acclimate to the
measured temperature (if different from the
ambient temperature).
Measurement of oxygen consumption rate
During experiments, individuals were maintained
in gas-tight glass syringes with volumes that were
adjusted for animal mass (Thuesen and Childress
1994). Syringes were placed in temperaturecontrolled water baths set at the temperatures
indicated in Table 1. Oxygen tension in the chambers
was measured by injecting a water sample into a
micro-respirometry chamber (75 ml sample volume)
connected to a polarographic oxygen sensor
maintained at the experimental temperature (Marsh
and Manahan 1999). Individual duration of experiments varied from 6 to 24 h. Oxygen tension in the
respirometry chambers never dropped below 50% air
saturation. The critical oxygen partial pressure (the
oxygen partial pressure above which the rate of
oxygen consumption is independent of oxygen
partial pressure) was determined for some species
by continuously recording oxygen in a sealed
chamber and was found to be 550% air saturation.
No relationship was observed between either final
oxygen tension or the duration of the experiment
and oxygen consumption rate.
For comparison at common temperatures,
rates were adjusted to 58C assuming a temperature
coefficient, Q10 ¼ (R2/R1)(10/T2T1), of 2.5. This value
is within the range typically occurring in the animals’
habitat. Significant differences between various
species and temperatures were determined by
analysis of covariance (ANCOVA, Statview inc.)
performed on relationships between oxygen consumption rate and body mass. Significance is at the
95% confidence level.
Metabolic rates of pteropod molluscs
883
Animal mass
Most animals were weighed on an analytical balance
and frozen for further analysis. Those that were
collected at sea were either frozen for subsequent
determination of mass on land, or were weighed on a
motion-compensated shipboard balance system
(Childress and Mickel 1980). Respiration rates are
reported in micromoles of O2 consumed per gram
wet weight per hour. Comparison with previous
studies variously requires that respiration rates be
expressed in terms of wet mass (WM), dry mass
(DM), ash-free dry mass (AFDM), and/or protein
content. Dry mass was determined for some species
in the present analysis by drying specimens at 608C
until constant weight (48 h). For Limacina helicina
antarctica, dried samples were then placed in a 5008C
muffle furnace for 12 h and weighed on a precision
analytical balance. The dry mass minus the ash
weight equals the AFDW. Shells were included in all
mass measurements. Wet mass was used as the
primary measure of size because it is the parameter
of physiological significance, i.e., it determines
constraints on animal locomotion, behavior, and
predator–prey interactions, among others. The use
of other parameters as indicators of size can lead
to misinterpretations of the biology of the whole
animal. The relative values of different expressions
of body size in this regard have been discussed
fully by Childress (1977) and Childress and
Somero (1979).
Results
Oxygen consumption rates
Mass-specific oxygen consumption rates (MO2, mmol
O2 g1h1) for 10 species of pteropods are presented
in Table 1. A range of sizes sufficient to determine
relationships between metabolism and body mass
was available only for a few species (MO2 ¼ aMb,
where a is a normalization constant, M is wet body
mass, and b is a scaling coefficient; see Figs. 1–3 for
equations). Among gymnosomes, mean oxygen
consumption rates ranged from 0.055 mmol
O2 g1h1 in Cliopsis krohni at 58C, to 40.94 mmol
O2 g1h1 in Pneumodermopsis spp., at 248C.
Once corrected for temperature differences,
assuming a Q10 of 2.5 and estimating effects of
body mass by comparing the normalization
constants of scaling relationships, the highest rates
were in C. antarctica (ANCOVA, P50.05), followed
by C. limacina and Pneumodermopsis (Fig. 3A).
Among thecosomes, rates were highest in tropical
Cavolinia spp. measured at 18 or 248C and lowest
in the gelatinous pseudothecosome, Corolla spp.
Fig. 1 Oxygen consumption rates (MO2, mmol O2 g1h1)
decline with wet body mass (M, g) according to the power
equation, MO2 ¼ aMb, where a is a normalization constant
independent of mass and temperature, and b is a scaling
coefficient that describes the slope of the relationship.
Temperature coefficients [Q10 ¼ (a1/a2)(10/(T2T1)] were determined from the normalization constants measured at different
temperatures. (A) Clione antarctica at 28C (open circles,
MO2 ¼ 0.84M0.29) and þ28C (closed circles, MO2 ¼ 1.50M0.23),
Q10 ¼ 4.26; (B) Clione limacina at 58C (open circles,
MO2 ¼ 0.58M0.43) and 108C (closed circles, MO2 ¼ 1.10M0.31),
Q10 ¼ 3.60. Normalization constants for C. antarctica at 2 and
28C are higher than are those of C. limacina at 10 and 58C,
respectively, suggesting that temperature compensation of some
energetically expensive physiological process is reflected in
whole-animal metabolic rates.
measured at 58C (Fig. 3B). Rates were roughly
equivalent
between
polar
(5.51 0.44 mmol
O2 g1h1) and temperate specimens of L. helicina
(6.36 0.87 mmol O2 g1h1) measured at the
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B. A. Seibel et al.
Fig. 2 Oxygen consumption rates (MO2, mmol O2 g1h1) as a
function of wet body mass (as in Fig. 1) for Clione antarctica at
28C (circles) and C. limacina at 58C (squares). Metabolic rates
of specimens captured where prey was abundant (fed, open
symbols) are higher than specimens deprived of food
[closed symbols; those either captured when prey were
absent (C. antarctica) or held in captivity for 1 week without
food (C. limacine)]. Regression equations for C. antarctica as
in Fig. 1 (fed) and MO2 ¼ 0.53M0.21 (food deprived).
temperatures of their respective habitats (2 and
58C). Temperature coefficients (Q10) were determined for C. limacina (Q10 ¼ 4.26, Fig. 1A) and
C. antarctica (Q10 ¼ 3.6, Fig. 1B) by comparing
normalization constants from scaling relationships.
Feeding history
Feeding history plays an important role in determining metabolic rates in pteropods. For thecosomes,
feeding-related variation was not adequately controlled in the present analysis, so we cannnot say
with certainty whether compensation for low temperature took place and cannot make precise
comparison with other studies. Because of their
monophagous nature, feeding is much more easily
controlled in gymnosomes and recent feeding history
in field-caught specimens can be roughly discerned
by the presence or absence of thecosomes at the time
gymnosomes were collected (Seibel and Dierssen
2003). Food deprivation resulted in a 30 and 50%
reduction in metabolic rate in C. limacina and
C. antarctica, respectively (Fig. 2).
Comparisons with published measurements
The present results are within the range reported
previously for species in each genus, despite very
Fig. 3 Oxygen consumption rates (MO2, mmol O2 g1h1) of
(A) gymnosomatous and (B) thecosomatous pteropods
normalized to 58C assuming a temperature coefficient, Q10,
of 2.5. (A) Clione antarctica (filled circles), Clione limacina
(open circles), Pneumodermopsis (plus symbol), Cliopsis krohni
(filled diamond), Notobranchea grandis (open triangles), and
Thliptodon spp. (open squares). (B) Limacina helicina antarctica
(filled circles), Limacina helicina (open circles), Cavolinia (plus
symbol), and Corolla spp. (filled triangles). Actively swimming
genera of predators (e.g., Clione) match those of their prey
(e.g., Limacina) and have rates 10-fold higher than those of
more sluggish predators (e.g., Cliopsis, Notobranchea, Thliptodon)
and their prey (e.g., Corolla).
different techniques of collection and measurement.
For example, respiration rates reported by Ikeda and
Fay (1981) for limited numbers of L. helicina
along the Antarctic Peninsula are similar to those
we obtained, but not directly comparable due to
large differences in body size of specimens in the two
885
Metabolic rates of pteropod molluscs
Antarctic regions (Seibel, personal observation).
Limacina helicina of comparable size, measured
at similar temperatures, fall within the range of
values we report here (Ikeda 1970, 1989). Smith and
Teal (1973) measured metabolic rates in L. helicoids
across a range of temperatures and hydrostatic
pressures and found that, below 108C, rates from
this deep-living species are unaffected by either
temperature or pressure. Those rates overlap with
our values for L. helicina. As we report here, Biggs
(1977) found that Corolla spp. has a much lower
metabolic rate than do euthecosomes such as
Cavolinia spp. Connover and Lalli (1974) presented
extensive measurements for C. limacina at a range of
temperatures that are consistent with our findings.
We hesitate to draw conclusions about temperature
compensation by comparing previously published
data to our own, however, because subtle differences
in body size, feeding history, and location of capture
of the specimens measured, as well as differences in
methods of collection and measurement, can greatly
influence such conclusions.
Swimming speed and behavior
Mean wing-beat frequencies were similar in
C. limacina (1.54 Hz, 108C) and C. antarctica
(1.36 Hz, 08C) (Borrell et al. 2005) at their respective
habitat temperatures. However, wing-beat frequency
declined significantly with body length (Fig. 4A) and
mean body length was greater in C. limacina.
Thus, at a common body size, C. limacina swam
nearly twice as fast at 108C as did C. antarctica
at 08C. Furthermore, wing-beat frequencies were
bimodal in C. limacina reflecting the multi-geared
swimming system in this species. No evidence of
different gears or gaits was observed in C. antarctica.
When disturbed, C. limacina displays a burst escape
response with wing-beat frequencies approaching
7 Hz (Satterlie and Spencer 1985), while C. antarctic
exhibits a strong full-body withdrawal reflex instead
(Borrell et al. 2005).
Body mass
Subsequently, we provide data on wet, dry, and ashfree-dry mass as well as content of protein and lipid
in select species so that others may make comparisons to previous studies. However, we refer only
to wet mass normalized rates throughout the
discussion because it is the parameter of physiological significance that determines constraints on
such parameters as locomotion, behavior, and
predator–prey interactions. For example, Clione
and Thliptodon may have similar metabolic rates
expressed as per-unit dry mass, but very different
ones when expressed as per-unit wet mass because
Thliptodon is much more gelatinous and, as a result,
is a very sluggish swimmer.
For C. antarctica, dry weights were linearly related
to wet weights (Dry weight ¼ 0.17 þ 0.13 Wet
Mass; R ¼ 0.99). In L. helicina, dry mass (DM)
was related to wet mass (M) as ln(DM) ¼
1.26 þ 0.87ln(M), ash-free dry weight is equal to
0.38ln(wet weight) þ 0.16, and wet mass (M) is
related to shell diameter (D) as M ¼ 0.53 þ
1.91lnD (R2 ¼ 0.86). Mean protein content was
4.0% of wet weight for L. helicina but only 3%
of wet weight for C. antarctica. When corrected for
the contribution of shell to wet weight (ash, 7%),
the protein content is much higher for L. helicina
than for C. antarctica. Using data on chemical
composition, including lipid content (5.08 and
0.5% wet weight for C. antarctica and L. helicina,
respectively (Phleger et al. 1997), the relative
densities of each species were determined. Limacina
helicina is negatively buoyant (1.18 g ml1), while
C. antarctica was nearly neutral (1.04 g ml1) relative
to sea water in McMurdo Sound (1.028 g ml1).
Discussion
Metabolism
The interspecific maintenance of physiological rates
across temperature gradients, popularly known as
‘‘metabolic cold adaptation,’’ has a long and controversial history (e.g. Addo-Bediako et al. 2002).
Whereas early studies may have over-estimated the
degree of temperature compensation due to problems
with experimental design (Scholander et al. 1953;
Wohlschlag 1960, 1964; Holeton 1974; Steffensen
2002), more recent studies point out theoretical flaws
in the concept of thermal compensation of wholeorganism metabolism (Clarke 1998). Specifically,
metabolic rates represent the sum of numerous
energetic expenditures and arbitrarily elevating cost
has no selective advantage (Clarke 1993). There is an
advantage, however, in increasing metabolic capacity
to a level consistent with required activity levels.
Routine and basal rates typically mirror active or
maximum sustainable rates (Reinhold 1999; Seibel
and Drazen 2007). To the extent that locomotory
costs are reflected in our routine measurements of
whole-animal oxygen consumption, we expected to
see elevated rates in actively swimming pteropods
permanently adapted to cold temperatures.
In support of this hypothesis, C. antarctica
measured at 2.08C have metabolic rates similar
to those of C. limacina measured at 58C.
886
B. A. Seibel et al.
Fig. 4 Wing-beat frequencies in polar and temperate clionids (A) as a function of body length (L, mm) in Clione antarctica [open circles;
1.4L0.5; 0 28C; Borrell et al. (2005)] and Clione limacina (closed circles; 2.4L0.62; 10 28C) during routine swimming (in the absence
of obvious external stimuli). (B) Wing-beat frequencies in C. limacina at 108C are bimodal with a peak representing slow swimming
using slow-twitch muscle fibers, and a second peak at higher frequencies that recruit fast-twitch muscle fibers, thereby augmenting
swimming power. (C) Clione antarctica at 08C swims at routine slow speeds of approximately 1 Hz, but lacks a fast swimming gear.
Similarly, C. antarctica measured at 28C have rates
equivalent to those of C. limacina measured at 108C
(Fig. 1A and B). However, an oxygen consumption
rate measured at 308C for a single unidentified
tropical clionid pteropod (Ikeda 1970) and our
own measurements of oxygen comsumption by
Pneumodermopsis spp. at 248C suggest that compensation is, at best, only partial. Assuming a Q10 of 2.5,
the normalization constant measured here for
C. antarctica at 2.08C (2.04) predicts a rate of
22.09 mmol O2 g1h1 at 248C. This value is within
the range of measurements on Pneumodermopsis,
but considerably higher than the 12.8 mmol
O2 g1h1 measured by Ikeda (1970). These results
are consistent with those of Torres and Somero
(1988) who demonstrated nearly complete compensation of metabolism in Antarctic fishes relative to
Californian species, but only partial compensation
relative to species from the warmer Gulf of Mexico.
The actual temperature coefficients measured here
were considerably higher than 2.5. For our data,
this may indicate that the rates measured
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Metabolic rates of pteropod molluscs
for C. antarctica at high temperatures, and for
C. limacina at low temperatures, could have been
elevated by the stress of being at temperatures
outside those occurring in their normal habitat.
in preparation; Dymowska et al., manuscript in
preparation) but may also result from kinematic
constraints associated with viscosity at low
temperatures (Borrell et al. 2005).
Swimming speed
Temperature compensation
Swimming speed, as indicated by wing-beat frequencies, does not appear to be fully temperaturecompensated (Fig. 4). Clione antarctica at 08C
swims with wing-beat frequencies similar to that
predicted for C. limacina by extrapolating to lower
temperatures (Fig. 4C). A Q10 of only 1.7 could
account for the difference in wing-beat frequency
between the two species. This is a much smaller
temperature effect than we observe for oxygen
consumption intraspecifically, suggesting at least
partial compensation in swimming speed. Nevertheless, wing-beat frequencies are lower in the
polar species, compared to temperate species, at
their respective habitat temperatures and body size.
This observation is in apparent conflict with our
hypothesized link between locomotory activity
and elevated rates of oxygen consumption in
C. antarctica. This discrepancy may be explained,
however, by fundamental constraints associated with
smaller size and low temperatures that require
different mechanisms for producing thrust (Borrell
et al. 2005). Furthermore, a multi-geared swimming
system in C. limacina appears to be absent in
C. antarctica. Clione limacina spontaneously switches
between distinct fast gears and slow gears during
routine swimming (Fig. 4B; Satterlie and Spencer
1985). Fast swimming is supported by additional
recruitment of a fast-twitch, mitochondria-poor
‘‘white’’ muscle equivalent, while slow swimming
relies principally on mitochondria-rich, slow-twitch
red muscle equivalent. A third gait, a ballistic burst
escape response, can be provoked by external
stimulation of the tail. In C. antarctica, the fast
and ballastic gaits appear to have been lost (Gilmer
and Lalli 1990; Borrell et al. 2005; Fig. 4A). Thus,
in our observations of ‘‘routine’’ swimming in
C. limacina, we have inadvertently counted wing
beats during both fast and slow swimming, the latter
of which may be partially supported anaerobically
and not entirely taken into account by measurements
of oxygen consumption. Clione antarctica displayed only the slower speed, believed to be entirely
supported by aerobic metabolism (Dymowska et al.,
manuscript in preparation). The apparent loss of
the capacity for fast swimming is, we believe,
due to physiological constraints within the neuromuscular system (Rosenthal et al., manuscript
As discussed by Clarke (1998), energy production by
mitochondria is generally constrained at low temperatures. Whereas significant rate-compensation
characterizes some enzyme systems (Somero 1995),
generation of mitochondrial ATP seems to be
constrained at low temperatures, perhaps due to
differing effects of temperature on processes relevant
for ion transport in mitochondria (Guderley 1998;
Johnston et al. 1998; Pörtner et al. 1998). In order
to generate higher output of power by their muscles,
cold-adapted organisms must compensate with
more mitochondria, increased concentration of
enzymes and/or greater surface area of the cristae
(Peck 2002; Pörtner 2002). Compensation may also
be achieved via recruitment of greater numbers of
aerobic muscle fibers, as the power output and
contraction rates of each muscle fiber are much
reduced and animals may not achieve their potential
performance at low temperatures (Bennett 1984;
Rome et al. 1984; Rome 1990).
Mitochondrial proliferation has been demonstrated in a variety of Antarctic fishes (Johnston
et al. 1998). In the sluggish Antarctic fish,
Pleuragramma antarcticum, for example, mitochondria occupy 56.3% of the volume of red muscle
fibers (Johnston et al. 1998) compared to a value of
32.4% for the red muscle fibers of skipjack tuna.
Wing muscles from C. antarctica show a dramatic
proliferation of mitochondria relative to C. limacina
(Dymowska et al., manuscript in preparation).
We believe, this is the primary cause of the elevated
rates of oxygen consumption we see in the
whole animal and is the basis for the observed loss
of the escape response in C. antarctica via displacement of fast-twitch muscle fibers.
Evolutionary ‘‘arms race’’
Evolutionary escalation of predator–prey interactions
is often described anthropomorphically as ‘‘arms
races.’’ For the interaction to endure, improved
capabilities in one species demands compensatory
improvements in the other (Brodie and Brodie
1999). However, coevolution requires that the
interaction between predator and prey be reciprocal.
This is rarely the case. The ‘‘life-dinner principle’’
suggests that predators may not respond
evolutionarily to prey adaptations because selection
888
in predator–prey interactions is typically asymmetrical (Brodie and Brodie 1999). If a predator fails
to capture its prey, it loses that meal (i.e., dinner)
but lives to hunt another day. Although the average
consequence of losing a prey may be strong
enough to drive an arms race, most predators can
simply switch to a more available prey species and
may experience higher fitness than if they had
captured the original prey. If, on the other hand,
the prey fails to escape, it loses its life and all
future fitness. The consequences of these interactions
are clearly more severe for prey. Exceptions to
this rule may exist in cases where predation on other
species is not possible.
Because gymnosomes are monophagous predators feeding exclusively on thecosomes, predator
and prey interactions may more closely approximate
a reciprocal relationship in pteropods. Thus, in
gymnosomes the evolution of mechanisms of capturing prey may respond directly to changes in the
strategy of avoiding predation on the part of their
thecosomatous prey. Here, we have observed a close
relationship between metabolic rates and locomotory
capacity in pteropod predators and their prey. For
example, Clione spp. and Pneumodermopsis spp.
swim continuously and engage in tactile foraging
for Limacina spp. and Cavolinia spp., respectively
(Lalli and Gilmer 1989). Rates of encountering prey
are presumably a direct function of swimming speed.
Upon encountering prey, buccal cones are everted
which strive to capture and manipulate the prey
shell. If this initial attempt is unsuccessful, however,
the thecosome prey evade predators via active
swimming (Harbison and Gilmer 1992). Not surprisingly, these animals have relatively high locomotory
capacity and metabolic rates relative to other
gelatinous zooplankton (Seibel and Drazen 2007).
In contrast, Cliopsis krohni and Thliptodon spp. are
among the slowest swimming gymnosomes (Lalli and
Gilmer 1989). They are much more gelatinous and,
at least in the case of Cliopsis, forage by making
direct contact with a prey species’ mucous feeding
web, rather than by contacting the prey itself. Cliopsis
attaches to the feeding web and is slowly pulled
toward its prey as the web is reabsorbed. They feed
predominantly, if not exclusively, on Corolla spp.
a slow-moving pseudothecosome. Both Corolla and
Cliopsis have metabolic rates at an order of
magnitude lower than those of the more active
pteropods described earlier (Fig. 3; Biggs 1977).
This reduction in metabolic rate is clearly accomplished, in part, by elevated water content in these
obviously gelatinous species. Gel plays an important
role in buoyancy (Seibel et al. 2004), allows
B. A. Seibel et al.
attainment of large size with little expense, and
may play a role in the provision of oxygen in some
species (Thuesen et al. 2005). However, reduced
locomotory demand associated with their foraging
strategy renders the accumulation of gel a costeffective strategy (Seibel et al. 2004; Webber and
O’Dor 2001).
Conclusions
The rates reported here for some species
(e.g., C. antarctica) are higher than for many other
gelatinous zooplankton of an equivalent size at a
similar temperature (Seibel and Drazen 2007). Just as
visual predation in the pelagic realm drives selection
for the highest metabolic rates among animals
(Childress 1995; Seibel et al. 1997; Seibel 2007;
Seibel and Drazen 2007), active predator–prey
interactions among the nonvisual pteropods is a
major factor in the evolution of their own high
metabolic capacity. Furthermore, the present results
reveal the power of this selection in overcoming
hypothesized constraints associated with body size
and temperature (Gillooly et al. 2001). Over the
range of organisms studied to date, temperature and
body size are relatively minor determinants of
metabolic rate. The ecological roles played by
organisms, and the associated energetic demands,
drive selection for high metabolic capacity.
Relaxation of this demand among sit-and-wait
predators allows them to take advantage of opportunities to save energy.
Thecosomatous pteropods are of considerable
ecological importance, reaching densities of thousands of individuals per cubic meter in some regions
(Pane et al. 2004). They are important components
of many ecosystems with a potential for influencing
phytoplankton stocks (Hopkins 1987), carbon export
(Noji et al. 1997), and dimethyl sulfide (DMS) levels
(Levasseur et al. 1994) that, in turn, influence global
climate through ocean-atmosphere feedback loops.
They are prey to a variety of important predators
besides gymnosomes, such as fishes, cephalopods,
and mammals among others (Lalli and Gilmer 1989).
As such, they are useful indicators of ecosystem
health in some regions (Seibel and Dierssen 2003).
Owing to rising atmospheric CO2 concentrations and
the acidification of ocean surface waters, the level of
calcium carbonate (CaCO3) in seawater is decreasing.
Surface waters of some regions (e.g., the Southern
Ocean) will become undersaturated within the next
50–100 years (Orr et al. 2005). Thecosome shells are
made of aragonite, a type of CaCO3 that is highly
soluble, which suggests that these organisms may
Metabolic rates of pteropod molluscs
be particularly sensitive to increasing CO2 and
reduced
concentrations
of
carbonate
ion.
Thecosome pteropods are the main planktonic
producers of aragonite in the world’s oceans.
Within parts of their present-day geographic
ranges, they will be the first major group of calcifying
organisms to be adversely effected by undersaturation of CaCO3 as a result of anthropogenic increases
in CO2 (Seibel and Fabry 2003; Drake et al. 2005;
Orr et al. 2005). Because of the strict relationship
between thecosomes and gymnosomes, the predator
will also be susceptible. Despite this anthropogenic
threat and the ecological importance of pteropods,
our understanding of their life cycles, distributions,
and general biology remains speculative (Kobayashi
1974; Gannefors et al. 2005). A major and immediate
change in carbon dioxide emissions may be required
to save the sea angels.
Acknowledgments
We thank the NSF Antarctic Biology Training
Course for providing the initial impetus for this
work. S. Haddock, K. Osborne, B. Robison,
F. Bezanilla, R. Levy, and Y. Arshavsky provided
valuable discussion and assistance in the field. We
thank the Monterey Bay Aquarium Research Institute
and the Captain and crew of the R/V Western Flyer
and pilots of the ROV Tiburon. We thank the staff at
Mcmurdo Station Antarctica, Mote Marine
Laboratory in Florida, and the Ocean Science
Center at Memorial University in Newfoundland
for field support. This research was supported in part
by NSF grants OPP-9980360 to R.D., OCE-0526493
and OPP-0538479 to B.A.S, and IBN-0344070 to
J.C.R. Further support was granted by NIH
NS039405-06, NCRR RCMI and G12RR03051 to
J.C.R, and a University of Rhode Island Faculty
Development Grant to B.A.S.
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