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High-speed video analysis of the escape responses of the Copepod Acartia tonsa to Shadows.

Abstract. The copepod Acartia tonsa exhibits a vigorous escape jump in response to rapid decreases in light intensity, such as those produced by the shadow of an object passing above it. In the laboratory, decreases in light intensity were produced using a fiber optic lamp and an electronic shutter to abruptly either nearly eliminate visible light or reduce light intensity to a constant proportion of its original intensity. The escape responses of A. tonsa to these rapid decreases in visible light were recorded on high-speed video using infrared illumination. The speed, acceleration, and direction of movement of the escape response were quantified from videotape by using automated motion analysis techniques. A. tonsa typically responds to decreases in light intensity with an escape jump comprising an initial reorientation followed by multiple power strokes of the swimming legs. These escape jumps can result in maximum speeds of over 800 mm ([s.sup.-1]) and maximum accelerations of over 200 m ([s.sup.-2]). In A. tonsa, phot ically stimulated escape responses differ from hydrodynamically stimulated responses mainly in the longer latencies of photically stimulated responses and in the increased number of power strokes, even when the stimulus is near threshold; these factors result in longer escape jumps covering greater distances. The latency of responses of A. tonsa to this photic stimulus ranged from a minimum of about 30 ms to a maximum of more than 150 ms, compared to about 4 ms for hydrodynamically stimulated escape jumps. Average response latency decreased with increasing light intensity or increasing proportion of light eliminated. Little change was observed in the vigor of the escape response to rapid decreases in visible light over a wide range of adaptation intensities.

Introduction

Planktonic copepods are an important link in marine food webs between microplankton and higher trophic levels. Copepods are well known for their vigorous escape responses (e.g., Singarajah, 1969; Fields and Yen, 1997), which play an important role in predator avoidance (e.g., Drenner et al., 1978; Viitasalo et al., 1998). These escape responses can be elicited by both hydrodynamic (Hartline et al., 1999; Kiorboe et al., 1999; Lenz and Hartline, 1999) and photic stimuli (Buskey et al., 1986, 1987). Despite the scarcity of direct evidence that chemosensory stimuli, by themselves, can produce vigorous escape responses in calanoid copepods, there is evidence that such stimuli can cause copepods to exhibit changes in swimming activity (e.g., Katona, 1973; Buskey, 1984). Predator-specific chemicals have also been shown to alter vertical migration behavior in freshwater zooplankton (e.g., Tjossem, 1990; Ringelberg, 1991) and marine crab larvae (Forward and Rittschof, 2000), but similar effects are yet to be demonstr ated in marine copepods (e.g., Bollens et al., 1994).

Light has long been known to have an important effect on the behavior of planktonic organisms, with much research emphasizing the effects of light on vertical migration (reviewed in Forward, 1988). Photophobic responses of copepods are thought to play a role in planktonic predator-prey interactions--both in terms of a predator-deterrent role of bioluminescence in dark-adapted copepods (Buskey and Swift, 1983, 1985) and in terms of a predator-avoidance role for copepods exposed to shadows in light-adapted copepods (Buskey et al., 1986). Alterations in behavior of planktonic organisms in response to decreases in light intensity have been demonstrated in neritic calanoid copepods (Buskey et al., 1987) and crab larvae (Forward, 1977).

Recent studies have used strain gauges and high-speed video to provide the high temporal resolution necessary to describe, in detail, the kinetics of the escape responses of both tethered (Lenz and Hartline, 1999; Hartline et al., 1999) and free-swimming (Buskey et al., 2002) calanoid copepods to hydromechanical disturbances. These studies demonstrate that copepod response latencies (down to 2 ms) are among the fastest ever recorded. This rapidity is in part due to the myelination of the nerves of some calanoid copepods (Davis et al., 1999), although extremely fast responses have also been found in Acartia tonsa (4 ms), which does not possess myelinated nerves (Buskey et al., 2002). In this study, we use high-speed video recording and computerized motion analysis techniques to describe the kinetics of the escape responses of the calanoid copepod A. tonsa to photic stimuli, and we compare the results to those of previous studies that examined the escape behavior of this species in response to hydrodynamic stim uli.

Materials and Methods

During March and April 2001, live zooplankton were collected from the University of Texas Marine Science Institute pier located in the Aransas Ship Channel connecting the Gulf of Mexico with Aransas and Corpus Christi bays. A 0.5-m diameter, l53-[micro]m-mesh plankton net was allowed to stream with the tidal current for 2-3 min. The contents of the cod end were diluted into a plastic bucket containing whole seawater and returned to the laboratory for sorting. The sample was examined under a dissecting microscope and adult male and female Acartia tonsa were removed using a wide-bore pipette. Twenty adults of a single sex were then placed in small, clear acrylic plastic aquaria (60 X 30 X 60 mm) containing filtered seawater. Each set of copepods was used in only one experiment. Before an experiment, the copepods to be used were allowed to adapt to a specific light intensity (100, 10, 1, 0.3 or 0.1 [micro]mol photons [m.sup.-2] [s.sup.-1]) for at least 1 h at near-ambient temperatures (19 [+ or -] 1[degrees]C fo r complete shadow experiments, 22[degrees]C for partial shadow experiments).

Experiments were performed in a darkroom, and redfiltered flashlights were used for viewing equipment and taking notes, since A. tonsa has a very low visual sensitivity to red light (Stearns and Forward, 1984a). For experiments testing the response of A. tonsa to complete shadows (adaptation light intensity reduced by 100%), a Dolan Jenner model 3100 Fiber Lite illuminator was used as the light source for the stimulus. A single light guide was oriented vertically above the aquarium containing the copepods, producing a beam of about 2.5-cm diameter on a sheet of opal glass resting on top of the aquarium. Light intensity was adjusted to produce a nominal light intensity of 100 [micro]mol photons [m.sup.-2] [s.sup.-1] as measured in air near the center of the aquarium; light intensity was measured using a LICOR LI-250 light meter with a LI-109A quantum sensor. The light was cut off using an electronic shutter for a period of 500 ms (Vincent Associates Uniblitz SD-10 shutter driver timer and model 255 shutter). L ight intensities of 10, 1, 0.3, and 0.1 [micro]moll photons [m.sup.-2] [s.sup.-1] were produced using a combination of neutral-density filters placed above the shutter at the tip of the light probe. The copepods were isolated from vibrational stimuli using a Newport bench-top vibration-isolating table.

In experiments where A. tonsa was subjected to partial reduction in light intensity, light was provided by a Dolan Jenner Model PL-180 quartz-halogen illuminator with dual branch light guides. The light beam from each branch of the light guide was directed from opposite sides at an angle of about 30[degrees] from vertical at the same area of opal glass directly over the small aquarium containing the copepods. One branch was fitted with the electronic Uniblitz shutter to cut off a fraction of the light striking the aquarium. The relative contribution of the light guides to total illumination of the chamber was modified using neutral-density filters. Only adult female copepods were used in studies of escape responses to partial reduction of light intensity.

In an experimental run, each group of copepods was allowed to further adapt to the new experimental setup for a minimum of 30 mm after being moved. The position of copepods in the field of view was observed on the television monitor, and the shutter was actuated when at least 2 copepods could be observed. After each group of copepods was stimulated, the high-speed video would be played back at slow speed (1 frame [s.sup.-1]) to record the number of copepods responding to the stimulus and the latency of the response. Each group of copepods was subjected to decreases in light intensity several times until a minimum of 20 copepods had been observed. These experiments were repeated with at least six different groups of copepods under each set of light-adaptation conditions.

Images of copepod escape responses were recorded at 1000 frames per second using a high-speed video camera (Kodak Motion Corder Analyzer Model SR-3000). The camera was equipped with a 50-mm fl.4 Nikon Nikkor lens, and viewed an area of about 25 X 30 mm. Additional lighting for recording copepod images during the absence or decrease of visible light during shadows was provided by a dark-field array of infrared-light-emitting diodes. The high-speed video camera recorded 2184 frames of video at 1000 frames per second. A signal from the electronic shutter was used to trigger the camera to capture half the video frames before and half after the decrease in light intensity. These frames were then played back at 30 frames per second and recorded on a Panasonic AG 6300 videocassette recorder.

These high-speed video records were then reviewed to choose escape paths for computerized motion analysis. Analysis of the behavioral parameters associated with the complete escape response of Acartia tonsa was hindered by the vigor of the response. To have the image of the copepods large enough to be automatically tracked by our motion analysis system, the field of view was limited to about 25 x 30 mm, and some copepods swam out of the field of view during their escape response. We attempted to quantify behavioral parameters for 20 escape responses for each set of conditions. We chose escape responses in which the copepod's initial position could be observed, and whose trajectories covered a minimum of one-third of the screen (tracked for at least 1 cm). Because escape behaviors were recorded in two dimensions, only trajectories perpendicular to the recording camera were accurately recorded. To minimize errors through analysis of paths not perpendicular to the camera, the aspect ratios of copepod images were measured at the beginning, middle, and near the end of their escape jumps (Buskey et al., 2002). Aspect ratios greater than 3 indicated that a copepod was nearly perpendicular to the line of view of the video camera. Escape responses with an aspect ratio less than 2.5 during part of their trajectory were not used for motion analysis. Since only 20 escape responses were quantified out of the more than 120 copepods observed, instances in which escape responses were recorded from the same copepod should be rare, if they occurred at all.

Swimming behavior of the copepods was quantified from videotapes using an Expertvision Cell-Trak video-computer motion-analysis system. High-speed video recorded at 1000 frames per second was transferred to videotape at 30 frames per second. These videotaped images of the copepods were digitized using the Motion Analysis VP-110 video-to-digital processor, and digitized outlines of the copepods were sent to a host computer at a rate of 30 frames per second. These digitized images were processed using Cell-Trak software to calculate the swimming speeds (mm [s.sup.-1]), acceleration (m [s.sup.-2]), and number of swimming leg thrusts per jump of the copepod's paths of travel. Jump latencies (time from stimulus to response) were determined by reviewing the videotapes frame-by-frame for a minimum of 200 ms. High-speed video analysis revealed an average delay of 6-ms between the signal sent to start the video sequence and the closing of the electronic shutter. Response latencies were corrected for this delay in sti mulus onset. A copepod occasionally performed a single spontaneous jump during the 200-ms period after the decrease in light intensity. Spontaneous jumps consist of a single thrust of the swimming legs with lower peak speeds than escape jumps (Buskey et al., 2002). These occurred both before and after the decrease in light intensity and were not counted as photic escape responses.

Results

Acartia tonsa responds to a rapid decrease in light intensity with a series of vigorous thrusts of the swimming legs. An example of a record of changes in swimming speed over time for the response of an adult female adapted to 100 [mu]mol photons [m.sup.-2] [s.sup.-1] and subjected to a complete reduction in visible light is shown in Figure 1. In this example, the dashed vertical line represents the time at which light intensity decreased; the response was initiated 32 ms later as a series of 11 thrusts of the swimming legs. Although the action was not apparent in the swimming speed record, examination of high-speed video revealed a rapid reorientation of the body axis by about 40 degrees during the 2-ms period preceding the first escape thrust. Maximum speeds during these swimming thrusts ranged between 400 and 600 mm [s.sup.-1], with minimum speeds between thrusts decreasing to between 200 and 350 mm [s.sup.-1]. The duration of each thrust of the swimming legs is about 8 ms (time from minimum speed at the beginning of one thrust to minimum speed at the beginning of the next thrust). The entire response lasted about 80 ms and displaced the copepod by about 31 mm. Examples of escape trajectories during photically stimulated escape jumps are shown in Figure 2A. These escape jumps, plotted from a common starting point, typically displace the copepod 10 to 15 mm from its original location. The range of responses observed, in terms of distance moved over time, ranges from 5 to 15 mm within the first 50 ms of the escape jump (Fig. 2B).

For complete reduction in light intensity, the proportion of copepods exhibiting an escape response varied with the light adaptation intensity. For adult male copepods, adaptation intensities of 0.3 [micro]mol photons [m.sup.-2] [s.sup.-1] and higher resulted in a response by about 80% of the copepods (Fig. 3A). For an adaptation intensity of 0.1 [micro]mol photons [m.sup.-2] [s.sup.-1], the response rate dropped rapidly to less than 10%. For adult females of A. tonsa the change in response rate with light adaptation intensity changed more gradually (Fig. 3B). At both 10 and 100 [micro]mol photons [m.sup.-2] [s.sup.-1], response rate was similar to that of males at the same intensity, about 80%. However, the response rate dropped to about 60% at 1.0 [micro]mol photons [m.sup.-2] [s.sup.-1] and to less than 50% at 0.3 [micro]mol photons [m.sup.-2] [s.sup.-1]. None of the females responded at an adaptation intensity of 0.1 [micro]mol photons [m.sup.-2] [s.sup.-1]. Therefore, the threshold light intensity for s timulating escape responses with complete shadows is between 0.1 and 0.3 [micro]mol photons [m.sup.-2] [s.sup.-1] for both adult males and females of A. tonsa.

For complete reduction in light intensity, the response latency between the initiation of the change in light intensity and the initiation of the first escape movement increases as the light adaptation intensity decreases (Fig. 3). For adult males, the mean response latencies progressively changed from 38 ms at 100 [micro]mol photons [m.sup.-2] [s.sup.-1] to 90 ms at 0.1 [micro]mol photons [m.sup.-2] [s.sup.-1]. A Kruskal-Wallis one-way ANOVA on ranks indicated a significant difference in response latencies at different adaptation intensities (P < 0.001). Dunn's method for pairwise comparisons revealed that all pairs of groups were significantly different from one another (P < 0.05). For adult females, the mean response latencies changed from 33 ms at 100 [micro]mol photons [m.sup.-2][s.sup.-1] to 96 ms at 0.3 [micro]mol photons [m.sup.-2] [s.sup.-1]. A Kruskal-Wallis one-way ANOVA on ranks again indicated a significant difference in response latencies at different adaptation intensities (P < 0.001). Pairwis e comparisons using Dunn's method indicated that latencies were significantly different from one another (P < 0.05) except for comparison of adaptation intensities of 0.3 and 1 [micro]mol photons [m.sup.-2] [s.sup.-1].

Although the response latencies changed for adult males of A. tonsa over the range of light adaptation intensities from 0.3 to 10 [micro]mol photons [m.sup.-2] [s.sup.-1], there was no evidence that the vigor of their escape behavior changed significantly until an adaptation intensity of 100 [mu]mol photons [m.sup.-2] [s.sup.-1] was applied (Fig. 4). Although no significant change in the number of swimming leg thrusts in each escape response was observed, there was a significant change in average speed (P < 0.001, one-way ANOVA, data not shown), maximum speed (P = 0.001, Kruskal-Wallis one-way ANOVA on ranks), and maximum acceleration (P < 0.001, one-way ANOVA). Pairwise comparisons revealed that average speeds and maximum accelerations of adult males during escape responses were significantly different at an adaptation intensity of 100 [mu]mol photons [m.sup.-2] [s.sup.-1] from those at each other intensity tested (Tukey test, P < 0.05). For maximum speed, adult male copepods adapted to 100 [mu]mol photons [m.sup.-2] [s.sup.-1] were significantly different only from those at 1.0 and 0.3 [mu]mol photons [m.sup.-2] [s.sup.-1] adaptation intensities (Dunn's method, P < 0.05).

Adult females of A. tonsa tested over a range of adaptation intensities from 0.3 to 100 [mu]mol photons [m.sup.-2] [s.sup.-1] also showed some differences in escape behaviors at the highest adaptation intensity (Fig. 5). There was no significant difference in the number of thrusts of the swimming legs in each escape jump (one-way ANOVA, P = 0.057) or in average speed of escape responses over this range of adaptation intensities (one-way ANOVA, P = 0.170, data not shown). For maximum speed during escape, there was a significant difference between escape responses of copepods adapted to different light intensities (Kruskal-Wallis one-way ANOVA on ranks, P = 0.04). Dunn's method for pairwise comparison for all pairs revealed that only the maximum speeds for escape responses of copepods adapted to 0.3 and 100 [mu]mol photons [m.sup.-2] [s.sup.-1] were significantly different (P < 0.05). For maximum acceleration achieved during escape responses, there was also a significant difference between copepods adapted to d ifferent light intensities (one-way ANOVA, P < 0.001). Pairwise comparison using Tukey's test revealed that copepods adapted to 100 [micro]mol photons [m.sup.-2][s.sup.-1] had significantly different maximum accelerations from each of the other adaptation intensities (P < 0.05).

Since no significant differences were found between between escape response parameters for copepods adapted to 10,1, or 0.3 [micro]mol photons [m.sup.-2][s.sup.-1], results from these three intensities were pooled for comparisons between male and female escape response parameters. Females had significantly longer response latencies than males, but significantly smaller initial turns (Table 1). Although there were no significant differences in the average escape speed of males and females, males exhibited significantly higher maximum speeds and maximum accelerations than females. Females also performed significantly more thrusts per escape jump than did males; the time between thrusts was longer and the minimum speed between thrusts was slower for females compared to males (Table 1). Overall duration of the escape jump was significantly longer for females, and the distance jumped was significantly farther for females than for males.

There was also a difference in the dominant directionality of the escape responses between copepods adapted to low light intensities (1 [micro]mol photons [m.sup.-2][s.sup.-1]) and higher adaptation intensities (100 [micro]mol photons [m.sup.-2][s.sup.-1]). Analysis of the direction of travel of the copepods during their high-speed escape responses reveals that for copepods adapted to low light intensities, the dominant swimming direction in response to a complete shadow was upward (Fig. 6B), whereas copepods adapted to higher light intensities showed a larger proportion of lateral swimming during escape responses (Fig. 6A).

For copepods exposed to only partial reductions in light intensity, which should correspond to light change more similar to a natural shadow in nature, the proportion of copepods responding to these changes in light intensity increased as the percent change in light intensity was increased (Fig. 7). For adult females adapted to a low light intensity (10 [micro]mol photons [m.sup.-2][s.sup.-1]), the proportion of copepods responding to light reductions dropped sharply from near 80% for a 100% reduction in light intensity to less than 10% for a 21% reduction in light intensity. For copepods adapted to higher light intensity (100 [micro]mol photons [m.sup.-2][s.sup.-1]), the proportion of copepods responding to reductions in light intensity declined more gradually from a response of 80% to a complete shadow to a response of less than 20% to a 21% shadow (Fig. 7). Response latencies did not change with percent light reduction in a systematic way. For adult females adapted to 10 [micro]mol photons [m.sup.-2][s.sup .-1]), there were significant differences in latency between copepods responding to 100%, 45%, and 28% reduction in light intensity (Kruskal-Wallis one-way ANOVA on ranks, P = 0.001). Too few copepods responded to a 21% reduction in light intensity to compare their latencies. Pairwise comparison to latencies at 100% reduction in light intensity showed that both groups differed significantly from this control group (Dunn's method, P < 0.05). For copepods adapted to 100 [micro]mol photons [m.sup.-2][s.sup.-1], there were also significant differences in response latencies between groups (Kruskal-Wallis one-way ANOVA on ranks, P < 0.001), and latencies for 45% and 28% reductions in light intensity were significantly different from control latencies for complete shadows, but there was no difference for 21% reductions (Dunn's method).

Discussion

Calanoid copepods are consumed by a wide range of pelagic predators including other copepods, chaetognaths, jellyfish, fish, and whales. Their primary sensory system for direct detection of predators is often considered to be mechanoreception; copepods are extraordinarily sensitive to small hydromechanical disturbances (Kiorboe and Visser, 1999; Lenz and Hartline, 1999). Photoreception may also play a role in predator avoidance by copepods. Most calanoid copepods, including Acartia tonsa, possess only a simple naplius eye consisting of paired dorsal ocelli and a single ventral ocellus (Elofsson, 1966). These simple photoreceptors are not capable of image formation, but photo-reception is thought to regulate the timing and extent of vertical migration in many copepod species (e.g., Stearns and Forward, 1984b; reviewed in Forward, 1988) which indirectly helps copepods avoid attack by visual predators by remaining in low light environments during daylight hours.

Calanoid copepods may use photoreception to avoid direct attacks by predators through photophobic responses to rapid increases or decreases in light intensity (Buskey et at., 1987). A commonly suggested function of the bioluminescence of dinoflagellates is as a deterrent against nocturnal predation (Tett and Kelly, 1973; Porter and Porter, 1979; Morin, 1983). Dark-adapted copepods exhibit strong escape responses to both natural and simulated dinofiagellate bioluminescence (Buskey et at., 1983; Buskey and Swift, 1983, 1985). Dinoflagellate bioluminescence stimulated during the feeding of copepods may attract visual predators on the copepods through a "burglar alarm" effect (Burkenroad, 1943; Mensinger and Case, 1992; Abrahams and Townsend, 1993). Light-adapted copepods exhibit similar escape responses when exposed to rapid decreases in light intensity (Buskey et at., 1986, 1987). These shadow responses might help copepods avoid "hydrocryptic" predators such as ctenophores and cnidarian medusae that produce onl y small hydrodynamic disturbances but cast shadows during the day as they descend in the water column.

To provide an effective defense against shadow-casting predators, it might seem that laterally oriented escape trajectories would be more effective than vertically oriented responses, which might propel the copepod toward the predator. In this study, copepods adapted to low light intensities more often showed vertically oriented escape paths, while those adapted to higher light intensities more often moved laterally (Fig. 6). In a previous study of shadow responses of Acartia tonsa from Narragansett Bay, Rhode Island, copepods adapted to these lower intensities showed laterally directed escape responses (Buskey et al., 1986). The reasons for the regional differences in behavioral responses of A. tonsa are uncertain. Coastal bays in Texas are generally shallower than Narragansett Bay and have weaker tidal currents (Hess and White, 1974; Armstrong, 1987). Members of this species are known to be strong vertical migrators (Stearns and Forward 1984b); in shallow subtropical bays they are closely associated with th e bottom during the day (Stubblefield et at., 1984; Buskey, 1993), rather than being suspended in the water column as they are in deeper environments with stronger currents. As a defense against shadow-generating benthic predators such as bottom-feeding fish, vertically directed escape responses might be effective adaptions for copepods closely associated with the bottom during the day.

Previous studies have used the same high-speed video analysis to examine hydrodynamically stimulated escape responses in A. tonsa (Buskey et al., 2002). One of the salient differences we found between the photically and mechanically triggered escape behaviors in this species was the substantially larger minimum reaction time of the former (29 ms vs. 3 ms to first movement; Tables 1, 2). The shortest photically triggered behavioral responses we have found in the invertebrate literature is about 30 ms for the startle response (mesothoracic leg thrust) to sudden light decreases in Drosophila melanogaster (review: Wyman et at., 1984). Larger animals are somewhat slower: 450 ms for the withdrawal reflex of leech (Laverack, 1969); 50 ms for the photic startle (flash) response of squid (Neumeister et at., 2000); and 30 ms for the photophobic fast-start response to sudden darkening in small fish (Hartline, unpubl. data). In contrast, the reaction latencies to mechanical stimulation of several species is considerably shorter: 40 ms for leech (Laverack, 1969); 11 ms for response to air puff in slowly walking cockroach (Camhi and Nolen, 1981); and 5 ms for the Mauthner-mediated fast-start in adult zebra fish (Eaton et al., 1977). Part of the reason for the difference between the two modalities is in the intrinsic speed of the sensory mechanism mediating the reaction. Mechanoreceptors in a wide variety of species employ direct mechanical links to transmit movement of the receptive surface (e.g., a seta) directly to the ion channel in the membrane of the receptor cell, thus reducing delays to onset of receptor potentials to tens of microseconds (e.g., Thurm, 1965; review: French, 1992). There is no need for time-consuming amplification beyond the initial molecular transduction event. Photic signals, on the other hand, involve an extensive biochemical cascade, including amplification of the original molecular event (photoisomerization of a rhodopsin-like compound) and diffusion of reactants to ionic channel sites in receptor membranes (review: Goldsmith, 1991). This takes time. Minimum latencies to onset of electrical changes are measured in milliseconds-10-20 ms in slow arthropod eyes, including most crustaceans; 3-6 ms in fast insect eyes (Bullock and Horridge, 1965); 7 ms in cuttlefish (Weeks and Duncan, 1974); 15-50 ms in cold-blooded vertebrates (Tomita, 1970, review and citations); 2 ms in monkey [at 38 [degrees]C], (Brown et al., 1965). Thus the photic modality is an inherently slow one, and the faster mechanical one has some clear advantages for animal survival.

A second component of the physiology impacting response characteristics is the neural substrate for processing the sensory information and firing the motorneurons associated with effector muscle action. Although differences of 10-20 ms in the primary transduction processes could account for much of the observed difference in behavioral latencies in copepods, they are perhaps not enough to account for all. Both in Drosophila and several annelids, the system of giant fibers (axons) is involved in both photically and mechanically triggered reactions. The large diameter of these axons speeds the conduction of nerve impulses and is widely used throughout invertebrate groups in escape and startle reactions. Vertebrates utilize myelination of axons instead of large size to increase conduction speed. Acartia is known to possess giant mechanosensory fibers in its antennae (Yen et al., 1992). It is not one of the myelinated species (Lenz et al., 2000). It may be presumed to have similar giant fibers involved in escape reactions elsewhere in its nervous system, as do other copepods (Lowe, 1935; Park, 1966; Lenz et al., 2000). However, the involvement of such elements is not yet certain in photic responses, and longer-latency pathways may be involved, as they are in the escape reactions of other organisms.

Several other aspects of photically triggered escape appeared different from those of the hydrodynamically triggered escape described by Buskey et al. (2002). Keeping in mind the intrinsic difficulties of inter-modality comparisons, we pooled the responses for copepods adapted to 0.3, 1, and 10 [micro]mol photons [m.sup.-2][s.sup.-1] adaptation levels going to complete dark, which were not significantly different from one another in their escape parameters, to compare with the range of hydrodynamic stimulation of Buskey et al. (2002). In addition, adaptation temperature was slightly different for responses compared in the two studies (19 [degrees]C in this study vs. 22 [degrees]C in Buskey et al., 2002), although there was no significant difference found in the response latencies of adult females of A. tonsa at 19 [degrees]C (Fig. 3) and 22 [degrees]C (Fig. 7) under the same light conditions. Maximum speeds in the photic responses were significantly higher for photically stimulated escape responses than for hydrodynamically stimulated responses in both male and female individuals of A. tonsa (Table 2). In contrast, maximum accelerations were significantly greater for hydrodynamically stimulated escape responses than for photically stimulated responses in both males and females. Photically stimulated reponses were also clearly more extensive than the hydrodynamically stimulated responses, with significantly more thrusts, longer jump duration, and greater distance jumped (Table 2). Interestingly, the duration of individual thrusts within an escape response was significantly greater for photically stimulated escapes for both males and females. The pattern that emerges from the various comparisons is that both the triggering of the escape (including the orientation component, and the excitation that keeps the neural circuits active) and the characteristics of the motor output are modality-specific. This calls into question the same central motor pattern generator being involved in both escape reactions. An increase in response vigor at the highest stimulus intensity was found in the present studies, but was not clearly apparent in our earlier work on mechanically evoked escape (Buskey et al., 2002). However, other copepods do appear to adjust the vigor of response with the intensity of mechanical stimulus (Lenz and Hartline, 1999), so this feature, too, may be parallel between photic and mechanosensory systems. It would seem that the two sensory-motor systems have evolved semi-independently, each to protect the animal from a certain type of predatory threat. In doing so, they utilize common elements of motor pattern production and control; yet rather distinct circuitry that gives characteristics appropriate to each situation has been developed as well. When examined minutely, the escape circuitry of other organisms has often revealed a multiplicity of pathways at the motor as well as the sensory side (e.g., Wine and Krasne, 1982; Eaton et al., 2001). It remains to be seen whether such complications also occur in copepod s.

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Table 1

Summary of escape response parameters for adult females and males of
Acartia tonsa exposed to photic stimuli

Parameter                                Females

Latency (ms)                       68.2 (1.8; 29-159)
Initial turn (deg)                 41.3 (3.3; 5-103)
Jump speed (mm [s.sup.-1])          256 (10; 125-476)
Maximum speed (mm [s.sup.-1])       446 (15; 235-827)
Max. acceleration (m [s.sup.-2])   93.3 (10.1; 54-156)
Number of thrusts                   7.5 (0.4; 3-15)
Minimum speed between thrusts (mm   130 (2.2; 65-230)
[s.sup.-1])
Thrust duration (ms)                8.8 (0.1; 4-13)
Jump duration (ms)                 74.6 (3.6; 33-136)
Distance jumped (mm)               12.5 (0.6; 5.3-25.5)

Parameter                                 Males             P

Latency (ms)                       62.2 (1.3; 35-138)    <0.001 *
Initial turn (deg)                 74.1 (4.6; 12-165)    <0.001 *
Jump speed (mm [s.sup.-1])          293 (12; 83-383)      0.453
Maximum speed (mm [s.sup.-1])       494 (16; 214-727)     0.002 *
Max. acceleration (m [s.sup.-2])    128 (6.0; 41-211)    <0.001 *
Number of thrusts                   4.9 (0.2; 2-9)       <0.001 *
Minimum speed between thrusts (mm   147 (3.2; 65-256)    <0.001 *
[s.sup.-1])
Thrust duration (ms)                8.1 (0.1; 6-14)      <0.001 *
Jump duration (ms)                 44.5 (1.8; 16-70)     <0.001 *
Distance jumped (mm)                8.6 (0.5; 3.4-15.1)  <0.001 *

Data are pooled for jumps with adaptation intensities of 10, 1, and 0.3
[micro]mol photons [m.sup.-2][s.sup.-1]. Means are based on 54 escape
jumps for females or 53 escape jumps for males. Standard error and range
are given in parentheses. Probability (P) is based on the Mann-Whitney
sum rank test.

An asterisk * indicates a significant difference ([alpha] = 0.05).

Table 2

Comparison of mean escape response parameters for adult males and adult
females of Acartia tonsa stimulated with photoic (PH) or hydrodynamic
(HY) stimuli

                                            Males                Females

Parameter                            PH     HY           P           PH

Response latency (ins)             62.2     3.6     <0.001 *       68.2
Initial turn (deg)                 74.1    82.1      0.22          41.3
Jump speed (mm [s.sup.-1])        293     213        0.09         256
Maximum speed (mm [s.sup.-1])     494     432        0.001 *      446
Max. acceleration (m [s.up.-2]    128     163       <0.001 *       93
Number of thrusts                   4.9     3.1     <0.001 *        7.5
Minimum speed between
  thrusts (mm [s.sup.-1])         147     166        0.272        130
Thrust duration (ms)                8.1     6.1     <0.001 *        8.8
Jump duration (ms)                 44.5    19.3     <0.001 *       74.6
Distance jumped (mm)                8.6     4.2     <0.001 *       12.5

                                      Females

Parameter                         HY           P

Response latency (ins)            3.5     <0.001 *
Initial turn (deg)               45.9      0.21
Jump speed (mm [s.sup.-1])      188       <0.001 *
Maximum speed (mm [s.sup.-1])   372       <0.001 *
Max. acceleration (m [s.up.-2]  112       <0.001 *
Number of thrusts                 3.3     <0.001 *
Minimum speed between
  thrusts (mm [s.sup.-1])       133        0.889
Thrust duration (ms)              6.6     <0.001 *
Jump duration (ms)               24.1     <0.001 *
Distance jumped (mm)              4.6     <0.001 *

Probability (P) based on the Mann-Whitney sum rank test.

An asterisk * indicates a significant difference ([alpha] = 0.05). Data
for responses to hydrodynamic stimuli are from Buskey et al. (2002).


Acknowledgments

This research was supported by the National Science Foundation through grant OCE 9910608. Cammie Hyatt and Becky Waggett assisted with sorting of copepods for experiments and with videotaping experiments. This is University of Texas Marine Science Institute Contribution Number 1246.

Received 7 June 2002; accepted 26 November 2002.

Literature Cited

Abrahams, M. V., and L. D. Townsend. 1993. Bioluminescence in dinofiagellates: a test of the burglar alarm hypothesis. Ecology 74: 258-260.

Armstrong, N. E. 1987. The ecology of open-bay bottoms of Texas: a community profile. U.S. Fish. Wildl. Serv. Biol. Rep. 85: 1-104.

Bollens, S. M., B. W. Frost, and J. R. Cordell. 1994. Chemical, mechanical and visual cues in the vertical migration behavior of the marine planktonic copepod Acartia hudsonica, J. Plankton Res. 16: 555-564.

Brown, K. T., K. Watanabe, and M. Murakami, 1965. The early and late receptor potentials of monkey cones and rods. Cold Spring Harbor Symp. Quant. Biol. 30: 457-482.

Bullock, T. H., and G. A. Horridge. 1965. Structure and Function in the Nervous Syste of Invertebrates. W.H. Freeman, San Francisco. 1719 pp. (Ch. 19).

Burkenroad, M. D. 1943. A possible function of bioluminescence. J. Mar. Res. 5:161-164.

Buskey, E. J. 1984. Swimming pattern as an indicator of the roles of copepod sensory systems in the recognition of food. Mar. Biol. 79: 165-175.

Buskey, E. J. 1993. Annual pattern of micro- and mesozooplankton abundance and biomass in a subtropical estuary. J. Plankton Res. 15: 907-924.

Buskey, E. J., and E. Swift. 1983. Behavioral responses of the coastal copepod Acartia hudsonica to simulated dinofiagellate bioluminescence. J. Exp. Mar. Biol. Ecol, 72: 43-58.

Buskey, E. J., and E. Swift. 1985. Behavioral responses of oceanic zooplankton to simulated bioluminescence. Bid. Bull. 168: 263-275.

Buskey, E. J., L. Mills, and E. Swift. 1983. The effects of dinoflagellate bioluminescence on the swimming behavior of a marine copepod. Limnol. Oceanogr. 28: 575-579.

Buskey, E. J., C. G. Mann, and E. Swift. 1986. The shadow response of the estuarine copepod Acartia tonsa. J. Exp. Mar. Biol. Ecol. 103: 65-75.

Buskey, E. J., C. G. Mann, and E. Swift. 1987. Photophobic responses of calanoid copepods: possible adaptive value. J. Plankton Res. 9: 857-870.

Buskey, E. J., P. H. Lenz, and D. K. Hartline. 2002. Escape behavior of planktonic copepods to hydrodynamic disturbances: high speed video analysis. Mar. Ecol. Frog. Ser. 235: 135-146.

Camhi, J. M., and T. G. Nolen. 1981. Properties of the escape system of cockroaches during walking. J. Comp. Physiol. 142: 339-346.

Davis, A. D., T. M. Weatherby, D. K. Hartline, and P. H. Lenz. 1999. Myelin-like sheaths in copepod axons. Nature 398: 571.

Drenner, R. W., J. R. Strickler, and W. J. O'Brien. 1978. Capture probability: the role of zooplankton escape in the selective feeding of planktivorous fish. J. Fish. Res. Board Can. 35: 1370-1373.

Eaton, R. C., R. A. Bombardieri, and D. L. Meyer. 1977. The Mauthner-initiated startle response in teleost fish. J. Exp. Biol. 66: 65-81.

Eaton, R. C., R.K.K. Lee, and M. B. Foreman. 2001. The Mauthner cell and other identified neurons of the brainstem escape network of fish. Prog. Neurobiol. 63: 467-485.

Elofsson, R. 1966. The nauplius eye and frontal organs of the non-Malacostraca (Crustacea). Sarsia 25: 1-128.

Fields, D. M., and J. Yen. 1997. The escape behavior of marine copepods in response to a quantifiable fluid mechanical disturbance. J. Plankton Res. 19: 1289-1304.

Forward, R. B., Jr. 1977. Occurrence of a shadow response among brachyuran larvae. Mar. Biol. 39: 331-341.

Forward, R. B., Jr. 1988. Diel vertical migration: zooplankton photobiology and behavior. Oceanogr. Mar. Biol. Annu. Rev. 26: 361-393.

Forward, R. B., Jr., and D. Rittschof. 2000. Alteration of photoresponses involved in diel vertical migration of a crab larva by fish mucus and degradation products of mucopolysaccharides. J. Exp. Mar. Biol. Ecol. 245: 277-292.

French, A. S. 1992. Mechanotransduction. Annu. Rev. Physiol. 54: 135-152.

Goldsmith, T. H. 1991. Photoreception and vision. Pp. 171-245 in Neural and Integrative Animal Physiology. C.L. Prosser, ed. Wiley-Liss, New York.

Hartline, D. K., E. J. Buskey, and P. H. Lenz. 1999. Rapid jumps and bioluminescence elicited by controlled hydrodynamic stimuli in a mesopelagic copepod, Pleuromamma xiphias. Biol. Bull. 197: 132-143.

Hess, K., and F. White. 1974. A numerical tidal model of Narragansett Bay. Sea Grant Marine Technical Rep. 20. University of Rhode Island, Kingston, RI.

Katona, S. K. 1973. Evidence for sex pheromones in planktonic copepods. Limnol. Oceanogr. 18: 574-583.

Kiorboe, T., and A. Visser. 1999. Predator and prey perception in copepods due to hydromechanical signals. Mar, Ecol. Prog. Ser. 179: 81-95.

Kiorboe, T., E. Saiz, and A. Visser. 1999. Hydrodynamic signal perception in the copepod Acartia tonsa. Mar. Ecol. Prog. Ser. 179: 97-111.

Laverack, M. S. 1969. Mechanoreceptors, photoreceptors, and rapid conduction pathways in the leech, Hirudo medicinalis. J. Exp. Biol. 50: 129-140.

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., D. K. Hartline, and A. D. Davis. 2000. The need for speed. I. Fast reactions and myelinated axons in copepods. J. Comp. Physiol. A 186: 337-345.

Lowe, E. 1935. On the anatomy of a marine copepod, Calanus finmarchicus (Gunnerus). Trans. R. Soc. Edinb. 63: 560-603.

Mensinger, A. F., and J. F. Case. 1992. Dinoflagellate luminescence increases susceptibility of zooplankton to teleost predation. Mar. Biol. 112: 207-210.

Morin, J. G. 1983. Coastal bioluminescence: patterns and functions. Bull. Mar. Sci. 33: 787-817.

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.

Park, T. S. 1966. The biology of a calanoid copepod Epilabidocera amphitrites McMurrich. Cellule 66: 129-251.

Porter, K. G., and J. W. Porter. 1979. Bioluminescence in marine plankton: a co-evolved antipredator system. Am. Nat. 114: 458-461.

Ringelberg, J. 1991. Enhancement of the phototactic reaction in Daphnia hyalina by a chemical mediated by juvenile perch (Perca fluviatilis). J. Plankton Res. 13: 17-25.

Singarajah, K. V. 1969. Escape reactions of zooplankton: avoidance of a pursuing siphon tube. J. Exp. Mar. Biol. Ecol. 3:171-178.

Stearns, D. E., and R. B. Forward, Jr. 1984a. Photosensitivity of the calanoid copepod Acartia tonsa. Mar. Biol. 82: 85-89.

Stearns, D. E., and R. B. Forward, Jr. 1984b. Copepod photobehavior in a simulated natural light environment and its relation to nocturnal vertical migration. Mar, Biol. 82: 91-100.

Stubblefield, C. L., C. M. Lascara, and M. Vecchione. 1984. Vertical distribution of zooplankton in a shallow turbid estuary. Contr. Mar. Sci. 27: 93-104.

Tett, P. B., and M. G. Kelly. 1973. Marine bioluminescence. Oceanogr. Mar. Biol. Annu. Rev. 11: 89-173.

Thurm, U. 1965. An insect receptor potential. Cold Spring Harbor Symp. Quant. Biol. 30: 83-94.

Tjossem, S. F. 1990. Effect of fish chemical cues on vertical migration behavior of Chaoborus. Limnol. Oceanogr. 35: 1456-1468.

Tomita, T. 1970. Electrical activity of vertebrate photoreceptors. Quart. Rev. Biophy. 3: 179-222.

Viitasalo, M, T. Kiorboe, J. Flinkman, L. Pedersen, and W. W. Visser. 1998. Predation vulnerability of planktonic copepods: consequences of predator foraging strategies and prey sensory abilities. Mar. Ecol. Prog. Ser. 175: 129-142.

Weeks, F. I., and G. Duncan. 1974. Photoreception by a cephalopod retina: response dynamics. Exp. Eye Res. 19: 493-509.

Wine, J. J., and F. B. Krasne. 1982. The cellular organization of crayfish escape behavior. Pp. 241-292 in The Biology of Crustacea Vol. 4, Neural Integration and Behavior, D.C. Sandeman and H.L. Atwood, eds. Academic Press, New York.

Wyman, R. J., J. B. Thomas, L. Salkoff, and D. G. King. 1984. The Drosophila giant fiber system. Pp. 133-161 in Neural Mechanisms of Startle Behavior, R.C. Eaton, ed. Plenum, New York.

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.

EDWARD J. BUSKEY (1), * AND DANIEL K. HARTLINE (2)

(1) Marine Science Institute, 750 Channel View Drive, Port Aransas, Texas 78373; and (2) Bekesy Laboratory of Neurobiology, Pacific Biomedical Research Center, University of Hawaii at Manoa, 1993 East-West Road, Honolulu, Hawaii 96822

* To whom correspondence should be addressed. E-mail: buskey@utmsi.utexas.edu
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Author:Buskey, Edward J.; Hartline, Daniel K.
Publication:The Biological Bulletin
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Date:Feb 1, 2003
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