Biol. Bull. 209: 75-85. (August 2005)
© 2005 Marine Biological Laboratory
Temperature Compensation in the Escape Response of a Marine Copepod, Calanus finmarchicus (Crustacea)
P. H. Lenz*,
A. E. Hower and
D. K. Hartline
Békésy Laboratory of Neurobiology, Pacific Biosciences Research Center, University of Hawaii at Manoa, 1993 East-West Rd., Honolulu, Hawaii 96822
* To whom correspondence should be addressed. E-mail: petra{at}pbrc.hawaii.edu
 |
Abstract
|
|---|
Calanus finmarchicus, the dominant mesozooplankter of the North Atlantic, is an important food source for many fishes and other planktivores. This species, which has limited diel vertical migration, depends on its fast-start escape response to evade predators. It has myelinated neuronal axons, which contribute to its rapid and powerful escape response. The thermal environment that C. finmarchicus inhabits ranges from below 0 °C to 16 °C. Previous studies have shown that respiration, growth, and reproductive rates are strongly dependent on temperature, with Q10 > 2.5. A comparable dependence of the escape response could place the animal at higher risk for cold-compensated predators. Our work focused on the temperature dependence of the behavioral response to stimuli that mimic predatory attacks. We found that in contrast to other biological processes, all aspects of the escape response showed a low dependence on temperature, with Q10 values below 2. This low temperature dependence was consistent for escape parameters that involved neural as well as muscle components of the behavioral response. These findings are discussed in the contexts of the predator-prey relations of copepods and the thermal dependence of behavior in other taxa.
|
Introduction
|
|---|
Temperature affects all biological processes from molecules to behavior. Seasonal and diel temperature fluctuations can be extensive. Compared to terrestrial organisms, aquatic, and especially oceanic, organisms experience more narrow temperature ranges. Nevertheless, temperature is a major factor in their ecological physiology and drives their population cycles. Physiologically based parameters, such as growth, reproduction, distribution, and behavior, of marine poikilotherms are affected by temperature. Many high-latitude species, such as the copepod Calanus finmarchicus, are adapted to low temperatures (< 4 °C). C. finmarchicus dominates the mesozooplankton in the North Atlantic from early spring to midsummer (Marshall and Orr, 1955). In the late summer and fall, these animals go through a diapause period as pre-adults, in copepodid stage five (CV), before maturing and re-initiating the population cycle in later winter to early spring. In its natural habitat, C. finmarchicus experiences a temperature range from below zero to over 15 °C, with optimal temperatures for population growth between 4 and 12 °C (Meise and O’Reilly, 1996; Hirche et al., 1997).
Interest in understanding and predicting population growth, distribution, and advection patterns have led to many field and experimental studies as well as to modeling efforts. Temperature, food quantity and quality, and predator abundance all contribute to observed spatial and temporal patterns (e.g., Meise and O’Reilly, 1996; Campbell et al., 2001; Dale et al., 2001). Temperature effects on growth and egg production are important components in models to predict the population dynamics of C. finmarchicus (e.g., Carlotti and Hirche, 1997). This species is a major food source for many North Atlantic fishes, and predation is another key factor in its population dynamics (e.g., Sullivan and Meise, 1996; Eiane et al., 2002). Temperature effects on predator-evasion behavior should thus be important in populations subjected to high predator abundances (Durbin et al., 1995b; Sullivan and Meise, 1996; Dale and Kaartwedt, 2000). To assess this possible impact, we examined the effects of temperature on the escape response of C. finmarchicus. The response consists of one or more propulsive "kicks" produced by the metachronal posterior-to-anterior sequence of posteriorly directed power strokes of the five pairs of thoracic pereiopods (Storch, 1929; Strickler, 1975). Escapes were elicited using a brief hydrodynamic stimulus, and the response was monitored with a force transducer and high-speed video. Parameters of the escape response were examined over a temperature range of 3 to 16 °C in an experimental period of 4 to 8 h.
|
Materials and Methods
|
|---|
Collection and maintenance of Calanus finmarchicus
Plankton were collected in Frenchman Bay off Mount Desert Island, Maine (44° 25.7' N, 66° 11.8' W) by towing a 0.5-m-diameter net (353-µm mesh) at a depth of about 5 m from a slowly moving boat. The collections were immediately diluted into 20-liter buckets and returned to the laboratory, where specimens of C. finmarchicus were sorted into 3.5- and 1.75-liter jars. The copepods were kept at 7 to 9 °C in a 12-h light-dark cycle. They were fed a mixture of Tetraselmis sp., Gymnodinium sanguinium (strain B4), Heterocapsa triquetra (strain HT984), and Oxyrrhis marina (strain CCMP1795) three times per week. A number of individuals molted from the copepodid five stage (CV) to adult in the time (up to 6 weeks) they were held in jars prior to the behavioral experiments. Only responsive individuals with intact antennae were used in the experiments.
Experimental setup
The setup for the behavior experiments has been described in detail elsewhere (Lenz and Hartline, 1999). Briefly, individual copepods were tethered to a force transducer with cyanoacrylate adhesive and transferred to the experimental dish. In the dish, the tethered copepod was positioned about 2 mm from the edge of a 3-mm-diameter sphere. The sphere was attached to a piezoelectric transducer (Burleigh PZL-060), which was computer-driven. The rapid vertical movement of this sphere produced a hydrodynamic disturbance, which decayed with distance from the center of the sphere following the principles of dipole spread (Gassie et al., 1993). The typical stimulus used in these experiments was a trapezoidally modulated 1.5-cycle sinusoid of 700 Hz, with a maximum vertical excursion of the sphere of 34 µm. The experimental animal was stimulated at 10-min intervals. If the animal did not respond with one or more kicks, it was stimulated again 1 min later with a larger hydrodynamic disturbance (3 x greater in magnitude). The magnitude first eliciting a response at any particular temperature was defined as threshold. In a few cases, the first reaction would be elicited at exceptionally high stimulus intensities, and it would be found that the animal thereafter would respond to much weaker stimuli. It was as if the strong stimulus served as a "wake-up call." In such cases, the weakest stimulus strength eliciting responses was taken as threshold. Once threshold was determined, the animal was tested again at 3 and 10 times threshold, allowing 10 min between tests. The suprathreshold tests were used to minimize the natural variability in responses that occurred near threshold and to provide some indication of the dependence of the responses on stimulus intensity. The reproducibility of responses to stimuli delivered at 10-min intervals or even less indicated that the recovery time allowed was adequate to avoid cumulative effects.
Temperature control
The experimental chamber was placed in a water bath used to control chamber temperature through the addition of ice. The initial experimental temperature was near the maintenance level (7 to 9 °C). In the initial phase of the experiment, the water temperature was cooled to below 5 °C. During the warming phase, multiple data points were obtained in the 7 to 9 °C range before allowing temperature to slowly rise to 15 °C. This warming phase typically lasted 2 to 3 h. It was followed by a phase of cooling to the original temperature range of 8 to 9 °C. This temperature was then maintained for 1 to 2 h, with responses monitored every 10 min. Behavior pattern progressions seen during the warming phase were encountered in reverse at about the same temperatures during the subsequent cooling phase. This protocol was used to assure that changes in behavior were related to temperature effects and not due to drift in the experiment.
Acceptance criteria
A total of 14 adult males, 4 adult females, and 10 pre-adults (stage CV) provided data of sufficient quality for at least partial analyses. Criteria for assessing experiment quality included high sensitivity to hydrodynamic stimulation (thresholds < 500 µm·s–1); consistent, short-latency (< 6 ms), strong responses (> 400 µN peak force); and complete, properly executed experimental testing over the full temperature range (5 to 15 °C), with return of responses to control patterns at the end of an experiment (8 to 9 °C). Experiments on 5 males and 1 stage CV fulfilled these criteria sufficiently that full analyses were made. The quantitative conclusions presented here are based on these individuals. These conclusions were confirmed qualitatively in the remaining animals.
Data analysis
Measurements performed on the force traces are indicated in Figure 1. Latency, or the time delay between the stimulus and the response, was measured as the time between the onset of the stimulus (time zero) and the force zero crossing at the beginning of the forward propulsive force, as shown in Figure 1 ("L"). Duration of the kick (ms) was measured as the time from the latency measurement to the end of the kick (Fig. 1, "D"). The end of the kick was characterized by a rapid change in slope and usually corresponded to the zero crossing. Maximum force (µN) was measured as peak force achieved during the kick (Fig. 1, "Max Force"). In some experimental animals, a high-frequency resonance in the transducer was generated by the pereiopod power strokes. In these cases, maximum force was measured to the midvalue of this high-frequency oscillation. Force rise time (ms) was measured as the time between the onset of the increase in force and the first peak (Fig. 1, "RT"). Force development rate (µN·s–1) was calculated as the ratio of the magnitude of the first clear peak in force divided by the rise time. Responses with multiple kicks were noted, and "kick" frequencies were calculated from the time between two consistent points in the peak force produced by a pair of pereiopods, usually the third pair ("Freq"; Fig. 1). As a convenient and conventional way of comparing temperature dependence among parameters and species, a Q10 value was calculated from the slope of a semilog plot of a given parameter, P, versus temperature, T:
 |
View larger version (14K):
[in this window]
[in a new window]
|
Figure 1. Force transient produced by a series of power strokes made by the pereiopods of a pre-adult stage CV individual of Calanus finmarchicus during an escape. Stim: arrow indicates onset of hydrodynamic stimulus produced by the vertical movement of a sphere of 1.5 cycle 700 Hz sine wave. Measurements made as indicated by bars: L (ms)—latency or response delay between time 0 and beginning of propulsive force; D (ms)—duration of force transient from initiation of propulsive force to the return to baseline; Max. F (µN)—maximum force produced during transient; RT (ms)—time delay between the onset of the propulsive force and the first peak; Freq (Hz)—reciprocal of the time (s) between successive force transients. The force transient shown was produced at 8 °C in response to a stimulus with amplitude 3 times threshold. The response had latency (L) of 2 ms, maximum force (Max. F) of 770 µN, force development rate (1st pk F/RT) of 180 µN·ms–1, kick duration (D) of 8.8 ms, and kick frequency (Freq) of 65 Hz.
|
|
Q10 indicates the factor by which a parameter changes for a 10 °C temperature change. It may be computed for a pair of temperature points (as we have done in presenting data obtained from text or figures in the literature in Tables 3 and 4) or, as with our present data, using a linear regression on log-transformed points over a range of temperatures. Technically, computation of a Q10 is founded in rate kinetics, but application of the formalism to nonkinetic parameters is widely used in the literature on thermal dependence of biological phenomena (e.g., Prosser, 1973), hence its application in the present paper.
|
Results
|
|---|
We typically collected C. finmarchicus at stage CV, and many of these molted into the adult stage during captivity. Adults obtained were mostly males, so only a few experiments were performed on adult females and stage CV individuals.
Ambient response profiles
At 8 to 9 °C, adult males usually responded to a hydrodynamic stimulus of up to 10 times threshold with a single escape kick, generated by the coordinated power strokes of the five pairs of pereiopods (Fig. 2). Occasionally, males would respond with multiple kicks (2 or 3) in quick succession (e.g., Fig. 5, 8 °C trace), or a second kick after a delay of 50 to 150 ms. Latencies varied with stimulus amplitude (see Fig. 4, open vs. closed symbols). For stimuli 3 times threshold, latencies or response delays in the adult males ranged from 2.8 to 3.6 ms. Maximum force, frequency of kicks, and duration of individual kicks did not change with stimulus amplitude. Measurements of these parameters were thus combined in the analyses. Duration of individual kicks was short, ranging from 8.7 to 12.6 ms, and the maximum force produced ranged from 580 to nearly 800 µN (Table 1). The force record for each kick typically registered three to four individual peaks, with the second or third peak producing the largest force (Fig. 2). These force peaks have been shown to correspond to power strokes of individual pereiopods (Alcaraz and Strickler, 1988; Lenz et al., 2004).
View larger version (27K):
[in this window]
[in a new window]
|
Figure 2. Force transients produced by a Calanus finmarchicus adult male in response to a hydrodynamic stimulus at 4 temperatures. Hydrodynamic stimulus: 1.5 cycle 700 Hz, amplitude: 3 times greater than threshold. Note enhanced resonance artifacts evoked by faster rise at higher temperatures.
|
|
View larger version (14K):
[in this window]
[in a new window]
|
Figure 5. Force transient duration as a function of temperature in a Calanus finmarchicus adult male. Hydrodynamic stimulus: 1.5 cycle 700 Hz, multiple amplitudes. 1/Q10 = 1.41; Experiment CF01-26.
|
|
View larger version (15K):
[in this window]
[in a new window]
|
Figure 4. Response latency to a hydrodynamic stimulus as a function of temperature in Calanus finmarchicus adult male. Open symbols and broken line: stimulus 3 times threshold (1/Q10 = 1.55). Solid symbols and line: stimulus 10 times threshold (1/Q10 = 1.56). The curves in this and the other temperature-dependence figures are fit to the equation
. Hydrodynamic stimulus: 1.5 cycle 700 Hz; Experiment CF01-26.
|
|
Compared to males, adult females and CVs showed a different pattern in escape behavior. Many of them were relatively non-responsive. Responses, even to very large stimuli, were limited to swimming with the feeding appendages or to very weak kicks with forces of 100–200 µN. Those females and CVs that were responsive produced long trains (20 or more) of pereiopod kicks in quick succession at frequencies of 30 to 70 Hz (Fig. 3). Maximum forces in these responsive individuals (females and CVs) ranged from 400 to over 1000 µN. Table 1 summarizes quantitative data for the single CV that fulfilled our acceptance criteria (CF00-02). We were unable to identify any features or conditions separating responsive from non-responsive animals.
View larger version (18K):
[in this window]
[in a new window]
|
Figure 3. Force transients produced in response to a hydrodynamic stimulus at 2 sets of temperatures showing the difference in response by an adult male (left) and a pre-adult stage CV (right) of Calanus finmarchicus. Hydrodynamic stimulus: 1.5 cycle 700 Hz, amplitude: 3 times greater than threshold. Note characteristic double escape pattern at 14 °C in the male, as well as weak transients from abortive kicks following strong initial response.
|
|
Sensitivity
Responsive animals reacted to the mechanical stimulus at all temperatures tested, but threshold was not constant. At the lower temperatures (below 11 °C), animals tended to be quiescent between trials, with only intermittent swimming using the feeding appendages and with thresholds as low as 250 µm·s–1. At the higher temperatures (above 11 °C), swimming with the feeding appendages was nearly continuous, with only short quiescent periods, and stronger stimuli were required to trigger escapes (Sign test, P = 0.0625; Siegel, 1956). We infer that the movements of the animal probably interfered with its detection of stimuli. Responses to the mechanical stimulus had shorter latencies, had faster rates of rise of propulsive force, and were more powerful at the higher temperatures (Fig. 2). Adult males increased their response by producing a second and sometimes even a third series of kicks after a pause of 50 to 150 ms (Fig. 3). Although we observed this type of response in 4 of the 5 experimental adult males at temperatures above 11–12 °C, the pattern was frequent in only one individual (20% of all responses). The number of kicks produced by C. finmarchicus CVs and adult females increased with temperature from 3 to 5 to over 20 above 12 °C (Fig. 3).
Latency
As the temperature increased, latency shortened, maximum force increased, and duration of the kick decreased. Between 3 and 16 °C, latencies declined by one-third (Fig. 4). Minimum latencies of 2 to 2.5 ms were measured in adult male and CV C. finmarchicus between 13 and 16 °C. However, even at 3 °C, the animals responded to the hydrodynamic stimulus in 4 ms or less. Q10 values calculated for latencies ranged from 1.2 to 1.6 for 6 different individuals (Table 2).
Kick kinematics
The rate of rise of propulsive force and, to a lesser extent, the duration of the kick are related to the speed of muscle contraction during the power strokes. Duration varied among individuals, from a minimum of 7.6 ms (CV, CF00-02) to 12.6 ms (adult male, CF01-09; Table 1). It declined with temperature (Fig. 5) with a Q10 of 1.3 to 1.5 (Table 2). In addition to the shortening of the kick at higher temperatures, the force transients increased in amplitude and fewer distinct peaks (2 or 3 instead of 4) were recorded (Fig. 2). High-speed video recording during two experiments (CF01-09, CF01-11) showed that changes in the shape of the force records correlated with changes in the pereiopod power strokes. Overall, the individual power strokes were faster, and often the strokes of two adjacent pairs of pereiopods came in quick succession with no decline in peak force in between. This was particularly true for the fourth, third, and second pereiopod pairs. In contrast, there was a delay between the power strokes of the second and first pereiopod pairs, which registered as a distinct final peak in the force record. With increased temperature (Fig. 6), maximum force increased with a Q10 value of 1.2 to 1.9 (Table 2). Force development rate increased with temperature as well (Fig. 7), with a Q10 value ranging from 1.3 to 2.0 (Table 2).
View larger version (14K):
[in this window]
[in a new window]
|
Figure 6. Maximum force as a function of temperature in a Calanus finmarchicus adult male. Hydrodynamic stimulus: 1.5 cycle 700 Hz, multiple amplitudes. Q10 = 1.41; Experiment CF01-26.
|
|
View larger version (16K):
[in this window]
[in a new window]
|
Figure 7. Force development as a function of temperature in a Calanus finmarchicus adult male. Hydrodynamic stimulus: 1.5 cycle 700 Hz, multiple amplitudes. Q10 = 1.78; Experiment CF01-27.
|
|
Frequency of kicks
As mentioned previously, adult males had a tendency to respond to the hydrodynamic stimulus with single kicks (66% to 100% responses in the five experiments). However, in three experiments, the individuals responded with double or triple kicks (16%, 22% and 34% of résponses). In these individuals and in the pre-adult C. finmarchicus (CV, Fig. 3), kick frequency increased as a function of temperature (Fig. 8, Table 2). At the lower temperature (< 8 °C), the kick rate was between 40 and 50 Hz (Fig. 8). At the highest temperatures tested (12 to 16 °C), multiple kicks in the males and the CV individual were produced at a frequency of 60 to 70 Hz. Q10 values ranged from 1.2 (CV) to 1.9.
View larger version (13K):
[in this window]
[in a new window]
|
Figure 8. Kick frequency as a function of temperature in a Calanus finmarchicus adult male. Hydrodynamic stimulus: 1.5 cycle 700 Hz, multiple amplitudes. Q10 = 1.73; Experiment CF01-27.
|
|
|
Discussion
|
|---|
Calanus finmarchicus occupies a central role in the North Atlantic ecosystem, and temperature is a key factor driving its population dynamics. Several previous studies of thermal effects have been made. In its natural habitat, C. finmarchicus typically experiences temperatures from 4 to 12 °C (Durbin et al., 1995a; Meise and O’Reilly, 1996; Gislason and Astthorsson, 2000; Dale et al., 2001). However, this species also occurs at temperature extremes below 0 °C (Head et al., 1999) and up to 18 °C (Turner et al., 1993). Temperature tolerance of C. finmarchicus is high in this range (Hirche, 1987), which covers the range we studied in the present experiments. Mortality rises sharply between 18 and 22 °C, with 50% mortality occurring at 20 °C (LT50) and 100% mortality at 22 °C (Hirche, 1987). Thermal stress response, as determined by the up-regulation of the heat shock protein hsp70, occurs at 18 °C for a prolonged exposure (48 h, Voznesensky et al., 2004).
Temperature exerts its effects on an organism through its relation to molecular motion. Physical properties derived from molecular interactions (e.g., phase transitions, membrane fluidity) and rates of biochemical reactions are usually the most important temperature-sensitive factors. Metabolic reaction rates typically show Q10 values of 2–2.5 (Prosser, 1973), and several biological functions have Q10 values in this range or above. Thus in C. finmarchicus, strong temperature dependence has been found for rates of growth (Q10 = 3.4 for dry weight: Campbell et al., 2001) and egg production (Q10 of ca. 5: Hirche et al., 1997). More closely related to behavior are effects on respiration. Within the copepod’s ecological range of 0 to 12 °C, Hirche (1987) found a Q10 of 3.3 for respiration. Table 3 shows Q10 values for various biological processes in C. finmarchicus. All those of a metabolically or biochemically reactive nature show a Q10 greater than 2.
View this table:
[in this window]
[in a new window]
|
Table 3 Effect of temperature on Calanus finmarchicus: comparison of Q10 values calculated for a variety of biological processes
|
|
Neuromotor components of escape
Interpreting quantitative measures of the thermal dependence of behavioral performance requires reference to the neuromotor mechanisms underlying the escape response. The production of an escape response in C. finmarchicus involves several temperature-dependent steps (e.g., Lenz and Hartline, 1999), including transduction of the hydrodynamic stimulus at the receptor cell membrane, encoding of the stimulus in a nerve-impulse barrage, propagation of the barrage along a chain of myelinated axons coupled by electrical synapses from sensory neurons to interneurons to motor neurons, and transmission across the chemical synapse at the neuromuscular junction where electrical activation of the muscle initiates the contraction that produces the pereiopod power stroke. Figure 9 illustrates this sequence and includes calculated values for the delays contributed by each step, at temperatures between 3 and 16 °C, based on measured values given in the literature for rapidly reacting poikilotherms. Two points emerge from this analysis. First, the observed reaction time at the higher temperatures is shorter (symbols and lower time scale, Fig. 9) by a factor of at least 2 than the time computed by summing all of the predicted delays for all of the steps (solid line and upper time scale, Fig. 9). Second, the low temperature dependence of the C. finmarchicus reaction time increases this discrepancy several-fold at low temperatures. Not only is this copepod much faster than can be accounted for on the basis of normal physiological parameters, but it is much better temperature-compensated than would be expected. Studies in other animals show that it is often not easy to explain the temperature dependence of burst-locomotion performance in terms of measurements of isolated neural and muscle function (Bennett, 1985; Table 4). Q10 values under 2 are reported for the jump speeds of frogs (Navas et al., 1999), for the C-start-mediated escape behavior of larval fishes (Batty and Blaxter, 1992; Table 4), and for the S-start of sculpin (Beddow et al., 1995; Table 4). In squid, behavioral measures such as rate of rise in intramantle pressure showed little dependence on temperature (6–12 °C) in intact animals, and peak pressure and maximum velocity achieved actually increased with decreasing temperature, suggesting a compensatory mechanism operating at a higher level in the nervous system (Neumeister et al., 2000; Rome et al., 2000). Compensation for temperature effects may include switching to alternative muscles and neural pathways at lower temperatures (Neumeister et al., 2000; Rome et al., 2000). The simplicity of the reflex circuitry in C. finmarchicus makes it difficult to envision alternative pathways. The range of Q10 values found in this species is comparable to or lower than that for escape performance in most poikilotherms (Table 4).
View larger version (28K):
[in this window]
[in a new window]
|
Figure 9. Components of delay contributing to reaction latency at different temperatures. Dashed lines show increments in values from each of the components labeled at the top, and the solid line shows the total, computed from values obtained from the literature ("Computed" time scale below). Symbols show minimum latencies observed in four experiments at each 1-degree interval from 3 °C to 16 °C ("Measured" scale). Diagram of the reflex chain shown at the bottom. Base values for delays used for each component, their determination temperature (in parentheses), and their Q10 values. Mechanosensory transduction: 200 µs (10 °C), Q10 = 2.1 (frog saccular hair cells: Corey and Hudspeth, 1983); encoding: 0.25 ms (15 °C, copepod (Labidocera) minimum spike latency: Yen et al., 1992), Q10 = 1.0 (cockroach tactile spine: French, 1985); conduction: 0.4 ms [4 mm at 10 m·s–1] (24 °C), Q10 = 1.8 (frog 10-µm-diameter myelinated axons: Bullock and Horridge, 1965); 2 electrical synapses: 0.4 ms (15 °C, crayfish lateral giant to motor giant neuron: Roberts et al., 1982), Q10 = 1.9 (crayfish segmental giant to motor giant neuron: Heitler and Edwards, 1998); neuromuscular junction delay: 1.3 ms (10 °C), Q10 = 3.1 (frog sartorius: Katz and Miledi, 1965), muscle activation 2.0 ms (17 °C, lobster antennular remoter muscle: Mendelson, 1969), Q10 = 2.2 (barnacle adductor muscle: Hagiwara et al., 1968). The origin of the twofold discrepancy in scale at low temperatures is unresolved. Exceptionally rapid neuromuscular junction and activation times may be involved. Abbreviations: in, interneuron; mn, motor neuron; nmj, neuromuscular junction; sn, sensory neuron.
|
|
Power-stroke repetition frequency is another parameter that is often neurally controlled. In land vertebrates, the thermal dependence of muscle twitch contractions is thought to limit repetition rates (Bennett, 1990). In aquatic organisms, movements are slowed by the greater density and viscous forces in the water. Generation of rhythmic motor patterns in nervous systems is typically an endogenous function of a "central pattern generator" circuit. Relative immunity to temperature changes has been described for burst generation in some isolated nervous systems, while sensitivity is high in others (Barker and Gainer, 1975; Anderson, 1976; Table 4). Our results indicate that the central pattern generator for multiple kicks in C. finmarchicus males, with an unknown contribution from sensory feed-back, is relatively insensitive to temperature shifts (Table 3).
Kick duration, maximum force, and force development rates are muscle-related processes. Rate processes in muscle (e.g., rate of force development) are more temperature-sensitive than force magnitude parameters (e.g., reviewed by Bennett, 1985, Bennett, 1990; Table 4), as the former are closely linked to molecular reactions (e.g., Mittenthal, 1975). As this general rule would dictate, copepod maximum force had a somewhat lower, albeit not significant, Q10 (Sign test, P = 0.19; Siegel, 1956) than did the rate of rise of force. These numbers were comparable to those found in vertebrates (Tables 3 and 4). Thus, although C. finmarchicus muscle is unusual in its speed (cycle rates of 40 to 50 Hz at 8–9 °C), its temperature dependence seems "conventional."
Ecological consequences of temperature compensation
The temperature range tested in our experiments is within the normal range that C. finmarchicus experiences in the Gulf of Maine. For many aquatic organisms, the challenge is maintaining high behavioral performance in the face of declining metabolic capabilities as temperature drops. This "temperature compensation" capability, as indicated by a low Q10 value, seems to have been achieved by C. finmarchicus adults and stage CV pre-adults in all parameters measured for the escape behavior. This would suggest that C. finmarchicus is well adapted to escape from predators at low temperatures. Population models do not usually incorporate changes in behavior as a function of temperature in predator-prey interactions (e.g., Fiksen and Folkvord, 1999; Fiksen and MacKenzie, 2002). Yet even small differences in the temperature-dependence of behavior can affect predator-prey outcomes in natural populations. Predator densities and hence predatory risk change seasonally. However, risk depends not only on predator density but also on seasonally varying changes in relative capture, and escape performance due to temperature effects. The complexity of this interaction has been demonstrated by Sell et al. (2001), who found increased ingestion rates with a decrease in temperature in one predator but not in another predator feeding on the same prey.
|
Acknowledgments
|
|---|
We thank Bob Campbell, Ted Durbin, Pat Hassett, and Melissa Wagner for assistance with algal cultures and information on maintenance of C. finmarchicus; Hinano Akaka, Brad Jones, Brian Kodama, Ted Murphy, and Gabriel Rodrigues for critical technical support; and the staff at Mount Desert Island Biological Laboratory (MDIBL) for assistance with logistics. We thank an anonymous reviewer for substantive suggestions for improvements of the original manuscript. This work was supported by the Salisbury Cove Research Fund of MDIBL and by National Science Foundation grant OCE 99-06223.
|
Footnotes
|
|---|
Received 10 January 2005; accepted 27 April 2005.
|
Literature Cited
|
|---|
Alcaraz, M., and J. R. Strickler. 1988. Locomotion in copepods: pattern of movements and energetics of Cyclops. Hydrobiologia 167/168:409–414.
Anderson, W. W. 1976. Endogenous bursting in Tritonia neurons at low temperature. Brain Res. 103:407–411.[Web of Science][Medline]
Barker, J. L., and H. Gainer. 1975. Studies on bursting pacemaker potential activity in molluscan neurons. II. Regulation by divalent cations. Brain Res. 84:489–500.
Batty, R. S., and J. H. S. Blaxter. 1992. The effect of temperature on the burst swimming performance of fish larvae. J. Exp. Biol. 170:187–201.[Abstract/Free Full Text]
Beddow, T. A., J. L. van Leeuwen, and I. A. Johnston. 1995. Swimming kinematics of fast starts are altered by temperature acclimation in the marine fish Myoxocephalus scorpius. J. Exp. Biol. 198:203–208.
Bennett, A. F. 1980. The thermal dependence of lizard behavior. Anim. Behav. 28:752–762.
Bennett, A. F. 1985. Temperature and muscle. J. Exp. Biol. 115:333–344.[Abstract/Free Full Text]
Bennett, A. F. 1990. Thermal dependence of locomotor capacity. Am. J. Physiol. Regul. Integr. Comp. Physiol. 259:R253–R258.[Abstract/Free Full Text]
Bullock, T. H., and G. A. Horridge. 1965. Structure and Function in the Nervous Systems of Invertebrates. W. H. Freeman, San Francisco. 1719 pp.
Burkhardt, D. 1959. Effect of temperature on isolated stretch receptor organ of the crayfish. Science 129:392–393.[Abstract/Free Full Text]
Burrows, M. 1989. Effects of temperature on a central synapse between identified motor neurons in the locust. J. Comp. Physiol. A 165:687–695.[Medline]
Campbell, R. G., M. M. Wagner, G. J. Teegarden, C. A. Boudreau, and E. G. Durbin. 2001. Growth and development rates of the copepod Calanus finmarchicus reared in the laboratory. Mar. Ecol. Prog. Ser. 221:161–183.
Carlotti, F., and H. J. Hirche. 1997. Growth and egg production of female Calanus finmarchicus: an individual-based physiological model and experimental validation. Mar. Ecol. Prog. Ser. 149:91–104.
Corey, D. P., and A. J. Hudspeth. 1983. Kinetics of the receptor current in bullfrog saccular hair cells. J. Neurosci. 3:962–976.[Abstract]
Dale, T., and S. Kaartvedt. 2000. Diel patterns in stage specific vertical migration of Calanus finmarchicus in habitats with midnight sun. ICES J. Mar. Sci. 57:1800–1818.
Dale, T., S. Kaartvedt, B. Ellertsen, and R. Amundsen. 2001. Large-scale oceanic distribution and population structure of Calanus finmarchicus, in relation to physical environment, food and predators. Mar. Biol. 139:561–574.
Durbin, E. G., A. G. Durbin, and R. C. Beardsley. 1995a. Springtime nutrient and chlorophyll a concentration in the southwestern Gulf of Maine. Cont. Shelf Res. 15:433–450.
Durbin, E. G., S. L. Gilman, R. G. Campbell, and A. G. Durbin. 1995b. Abundance, biomass, vertical migration and estimated development rate of the copepod Calanus finmarchicus in the southern Gulf of Maine during late spring. Cont. Shelf Res. 15:571–591.
Eiane, K., D. L. Aksnes, M. D. Ohman, S. Wood, and M. B. Martinussen. 2002. Stage-specific mortality of Calanus spp. under different predation regimes. Limnol. Oceanogr. 47:636–645.
Fiksen, Ø., and A. Folkvord. 1999. Modelling growth and ingestion processes in herring larvae (Clupea harengus L.). Mar. Ecol. Prog. Ser. 184:273–289.
Fiksen, Ø., and B. R. MacKenzie. 2002. Process-based models of feeding and prey selection in larval fish. Mar. Ecol. Prog. Ser. 243:151–164.
French, A. S. 1985. The effects of temperature on action potential encoding in the cockroach tactile spine. J. Comp. Physiol. A 156:817–821.
French, A. S., and J. E. Kuster. 1982. The effect of temperature on mechanotransduction in the cockroach tactile spine. J. Comp. Physiol. A 147:251–258
Gassie, D. V., P. H. Lenz, J. Yen, and D. K. Hartline. 1993. Mechanoreception in zooplankton first antennae: electrophysiological techniques. Bull. Mar. Sci. 53:96–105.
Gislason, A., and O. S. Astthorsson. 2000. Winter distribution, ontogenetic migration, and rates of egg production of Calanus finmarchicus southwest of Iceland. ICES J. Mar. Sci. 57:1727–1739.
Hagiwara, S., K. Takahashi, and D. Junge. 1968. Excitation-contraction coupling in a barnacle muscle fiber as examined with voltage clamp technique. J. Gen. Physiol. 51:157–175.[Abstract/Free Full Text]
Head, E. J. H., L. R. Harris, and B. Petrie. 1999. Distribution of Calanus spp. on and around the Nova Scotia Shelf in April: evidence for an offshore source of Calanus finmarchicus to the central and western regions. Can. J. Fish. Aquat. Sci. 56:2463–2476.
Heitler, W. J., and D. H. Edwards. 1998. Effect of temperature on a voltage-sensitive electrical synapse in crayfish. J. Exp. Biol. 201:503–513.[Abstract/Free Full Text]
Hirche, H.-J. 1987. Temperature and plankton. II. Effect on respiration and swimming activity in copepods from the Greenland Sea. Mar. Biol. 94:347–356.
Hirche, H.-J., U. Meyer, and B. Niehoff. 1997. Egg production of Calanus finmarchicus: effect of temperature, food and season. Mar. Biol. 127:609–620.
Höger, U., and A. S. French. 1999. Temperature sensitivity of transduction and action potential conduction in a spider mechanoreceptor. Pflüg. Arch. Eur. J. Physiol. 438:837–842.[Web of Science][Medline]
Jaslove, S. W., and P. R. Brink. 1986. The mechanism of rectification at the electrotonic motor giant synapse of the crayfish. Nature 323:63–65.[Medline]
Katz, B., and R. Miledi. 1965. The effect of temperature on the synaptic delay at the neuromuscular junction. J. Physiol. 181:656–676.[Free Full Text]
Lenz, P. H., and D. K. Hartline. 1999. Reaction times and force production during escape behavior of a calanoid copepod, Undinula vulgaris. Mar. Biol. 133:249–258.
Lenz, P. H., A. E. Hower, and D. K. Hartline. 2004. Force production during pereiopod power strokes in Calanus finmarchicus. J. Mar. Syst. 49:133–144.
Llinas, R., M. Sugimori, and K. Walton. 1987. Further studies on depolarization release coupling in squid giant synapse. Adv. Exp. Med. Biol. 221:1–17. (cited in Rosenthal and Bezanilla, 2000)
Marshall, S. M., and A. P. Orr. 1955. The Biology of a Marine Copepod Calanus finmarchicus (Gunnerus). Oliver & Boyd, Edinburgh. 188 pp.
Meise, C. J., and J. E. O’Reilly. 1996. Spatial and seasonal patterns in abundance and age-composition of Calanus finmarchicus in the Gulf of Maine and on Georges Bank: 1977–1987. Deep-Sea Res. II 43:1473–1501.
Mendelson, M. 1969. Electrical and mechanical characteristics of a very fast lobster muscle. J. Cell Biol. 42:548–563.[Abstract/Free Full Text]
Mittenthal, J. E. 1975. A sliding filament model for skeletal muscle: dependence of isometric dynamics on temperature and sarcomere length. J. Theor. Biol. 52:1–16.[Web of Science][Medline]
Moffett, S., and H. Wachtel. 1976. Correlations between temperature effects on behavior in Aplysia and firing patterns of identified neurons. Mar. Behav. Physiol. 4:61–74.
Navas, C. A., R. S. James, J. M. Wakeling, K. M. Kemp, and I. A. Johnston. 1999. An integrative study of the temperature dependence of whole animal and muscle performance during jump and swimming in the frog Rana temporaria. J. Comp. Physiol. B 169:588–596.
Neumeister, H., B. Ripley, T. Preuss, and W. F. Gilly. 2000. Effects of temperature on escape jetting in the squid Loligo opalescens. J. Exp. Biol. 203:547–557.
Prosser, C. L. 1973. Temperature. Pp. 362–428 in Comparative Animal Physiology, 3rd ed. C. L. Prosser, ed. Saunders, Philadelphia.
Ritchie, J. M., and D. Stagg. 1982. A note on the influence of potassium conductance (gK) on conduction velocity in myelinated fibres. J. Physiol. 328:32P–33P.
Roberts, A. M., F. B. Krasne, G. Hagiwara, J. J. Wine, and A. P. Kramer. 1982. The segmental giant: evidence for a driver neuron interposed between command and motor neurons in the crayfish escape system. J. Neurophysiol. 47:761–781.[Abstract/Free Full Text]
Rome, L. C., D. M. Swank, and D. J. Coughlin. 2000. The influence of temperature on power production during swimming. II. Mechanics of red muscle fibres in vivo. J. Exp. Biol. 203:333–345.
Rosenthal, J. J. C., and F. Bezanilla. 2000. Seasonal variation in conduction velocity of action potentials in squid giant axons. Biol. Bull. 199:135–143.[Abstract]
Sell, A. F., D. van Keuren, and L. P. Madin. 2001. Predation by omnivorous copepods on early developmental stages of Calanus finmarchicus and Pseudocalanus spp. Limnol. Oceanogr. 46:953–959.
Siegel, S. 1956. Nonparametric Statistics for the Behavioral Sciences. McGraw-Hill, New York. 312 pp.
Storch, O. 1929. Die Schwimmbewegung der Copepoden, auf Grund von Mikro-Zeitlupenaufnahmen analysiert. Verh. Dtsch. Zool. Ges. Zool. Anz. Suppl. 4:118–129.
Strickler, J. R. 1975. Swimming of planktonic Cyclops species (Copepoda, Crustacea): pattern, movements and their control. Pp. 599–613 in Swimming and Flying in Nature, 2, T.Y.T. Wu, C.J. Brokaw, and C. Brennen, eds. Plenum Press, New York.
Sullivan, B. K., and C. J. Meise. 1996. Invertebrate predators of zooplankton on Georges Bank, 1977–1987. Deep-Sea Res. II 43:1503–1519.
Turner, J. T., P. A. Tester, and J. R. Strickler. 1993. Zooplankton feeding ecology: a cinematographic study of animal-to-animal variability in the feeding behavior of Calanus finmarchicus. Limnol. Oceanogr. 38:255–264.
Voznesensky, M., P. H. Lenz, C. Spanings-Pierrot, and D. W. Towle. 2004. Genomic approaches to detecting thermal stress in Calanus finmarchicus (Copepoda: Calanoida). J. Exp. Mar. Biol. Ecol. 311:37–46.
Yen, J., P. H. Lenz, D. V. Gassie, and D. K. Hartline. 1992. Mechanoreception in marine copepods: electrophysiological studies on the first antennae. J. Plankton Res. 14:495–512.[Abstract/Free Full Text]
This article has been cited by other articles:
|
|
|
|
 
S. M. Hunt, M. Elvin, S. K. Crosthwaite, and C. Heintzen
The PAS/LOV protein VIVID controls temperature compensation of circadian clock phase and development in Neurospora crassa
Genes & Dev.,
August 1, 2007;
21(15):
1964 - 1974.
[Abstract]
[Full Text]
[PDF]
|
|
|
TOP
Abstract
Introduction
