The Development of Copepod Capture Strategies in
Juvenile Squid, Loligo opalescens
Donald S. Chen
William F. Gilly
September 22, 1994
I Abstract:
Juvenile squid, Loligo opalescens, face a great challenge in catching quick, elusive
copepods. The mastery of copepod capture, an acquired ability, develops progressively
past a basic attack strategy, through various strategies which facilitate capture, namely the
"arm-intercept" and the "tentacular grab." Squid raised exclusively on easily captured
Artem ia nauplii and introduced to a copepod diet 40 days after hatching could not master
copepod capture and died, presumably of starvation.
II. Introduction:
Juvenile squid are active predators with high metabolic rates sustained by
consuming as much as 35-80% of their body weight each day (Hurley, 1976). Little is
known about the life history of juvenile squid, such as where they are found or what they
eat-one can naturally speculate that they prey upon copepods, among other species, to
obtain their nourishment. In captivity, hatchling squid vigorously hunt and attack
copepods (Hurley, 1976), a major component of marine plankton, and it is likely that
copepods are a main food source in the wild as well.
Because copepods are small, erratically moving creatures with an extremely quick
escape response triggered by the motion of nearby predators (Yen & Fields, 1992), capture
of these organisms is a definite challenge for a newly hatched squid. Thus, we may ask,
what performance modifications occur in squid, as their motor capabilities develop after
birth, so that they may be more successful in copepod captures.
As Hurley (1976) described, young L. opalescens, in their attacks on Artemia
nauplii, copepods, and larval fish, display three distinct sequential attack behaviors:
attention, positioning, and seizure. This paper builds upon this earlier work, through a
more in depth study of attacks on copepods, a major prey type which is the same as those
squid hatchlings encounter in the wild, and by focusing on the ontogeny of this complex
behavior.
Hanlon and Hixon (1983) characterized a wave of mortality during the first two
weeks post-hatching, due to squid that fail to properly initiate feeding behavior. This
work focuses on prey capture behavior after this initial period of mortality, by squid
which have presumably acquired the most basic skills to feed.
Development of copepod prey capture behavior was examined through the
simultaneous rearing of two experimental groups. Whereas copepods were fed to the one
group of squid shortly after birth, only slow, easily captured Artemia nauplii were fed to
the other group of squid from birth until day 40. On day 40, Artemia feeding ceased, and
these squid were thereafter fed copepods only. This experimental design allowed us not
only to observe the developing prey capture techniques in squid exposed to copepods from
birth, but also to compare the success and quality of copepod attacks between these squid
and the non-challenged, Artemia-fed squid. Study of the impaired attacks by Artemia-fed
squid provided additional insight into the nature of successful copepod captures.
Results from these two experiments suggest that first, copepod-capture is an
acquired ability developing through a progression of attack strategies, and second, a
window of opportunity exists early in life for squid to master copepod capture.
Results of this study may be relevant to foraging behavior in the field, and thereby
be important to fisheries biology. In addition, findings from this study will serve to guide
approaches to squid mariculture in the optimal design of feeding regimens. Finally, the
characterization of specific behaviors revealed at certain ages in this study may provide a
valuable model system for developmental neurobiology studies in relation to experience¬
dependent modification of behavior.
IIi. Matenals anò Memoûs:
Culture:
Five egg cases of the California market squid, species Loligo opalescens were held
at the Monterey Bay Aquarium in each of two identical 320 liter tanks. Each of the tanks,
labelled tank two and tank three, represented an experimental group, hereafter referred to
as group two and group three, respectively. These black cylindrical tanks possess gently
sloping conical bottoms and measure one meter in diameter at the top. Tanks were
exposed to natural daylight that entered the room, and overhead fluorescent lights
illuminated the tanks between 6 a.m. and 6 p.m. daily. Except for periods of maintenance
and feeding, the tanks were kept partially covered with a black plastic sheet. Each
morning, all dead squid were siphoned out of the tank, and the daily mortality count was
tabulated. Detritus was also siphoned off the bottom and organic debris skimmed from
the surface at this time.
Flow-through water was provided to the tanks from a temperature-controlled
reservoir (-300 liters volume) fed with natural seawater passed through a 10 micron filter,
and water recirculated into the tanks. Egg cases were held at 14-15°C. until hatching,
after which the temperature was increased by approximately 0.6 °C. per day until 17-
18°C. was reached. Once the hatching commenced, the eggs were removed after several
days, and day one post-hatching was assigned to the day of most significant hatching
activity.
Feeding:
Squid hatchlings were fed once daily with either Artemia nauplii enriched with
algae and Super Selco (a nutrient medium rich in lipids, fatty acids, and vitamins;
produced by Artemia Systems N.V., Belgium), or with live marine plankton, obtained by
conventional surface tows in Monterey Bay, that consisted primarily of small, very quick,
Acartia sp. copepods, although larger Calanoid sp. copepods, chaetognaths, and an
assortment of crustacean larvae were also present in significant numbers.
Group two hatchlings (those in tank two) were fed marine plankton when available,
and Artemia nauplii when plankton was not available. Group three hatchlings were fed
only Artemia nauplii until day 40, when their diet was switched permanently to wild
plankton. Fig. 1 details the feeding regimen for each tank and presents daily mortality
counts. Two waves of mortality occur over days 1-12 and 25-35 in both groups, and this
is commonly seen in squid rearing operations (Hanlon & Hixon, 1983). The large
numbers of deaths in Group three starting on day 40 is discussed below.
Filming:
Feeding behavior was recorded with a Canon Al Digital Hi8 camcorder fitted with
a f 1 Vivatar close up lens and mounted on a tripod. The camcorder filmed at 30 frames
per second with a shutter speed of 1/60 second. Floodlights provided supplemental
lighting. With the camcorder elevated on the tripod and turned downward, filming
occurreò at an angle àmost perpendicular to me surface oi me water. » ên mummateò
squid displaying attack behavior were selectively tracked while filming until the squid
either successfully caught the prey item, stopped attacking, or moved out of the focal
range of the camcorder. Each filming session lasted approximately half an hour. Due to
the fluctuating availability of copepods, attacks on copepods were not filmed on every
day.
Frame-by-frame analysis of the data was undertaken using a Sony 9700 Hi 8
editing deck and a Sony Trinitron video monitor. Total attack distance and maximum
attack speed were measured using a caliper precise to .001 inch and normalized to the
mantle length of the attacking squid. Attack distance refers to the apparent straight-line
distance between the tip of the squids' arms and the copepod on the last frame just before
the squid's arms began to open up to initiate the actual attack. Maximum, or peak, attack
speed was measured on the monitor as the greatest distance travelled by the squid between
two consecutive frames during the attack lunge. Peak speed was usually attained within
four frames and represents the final approach of the squid, for after this burst of speed,
either the squid closed its arms upon the copepod in the culmination of a successful
attack, or the copepod escaped from the squid (an unsuccessful attack). Attacks in which
the squid was obviously moving vertically to a significant extent were not included in the
analysis. Direction of attack and copepod escape direction were also recorded when they
could be unambiguously determined by the orientation of the copepod antennae.
IV. Results:
The Basic Attack Sequence:
In the most general attack strategy observed (Fig. 2), the squid first fix their
attention upon and orient towards the potential copepod prey, pointing their arms in a
cone directly at the copepod. The squid actively maintains this posture through rhythmic
jetting and presumably fin control to remain in a fixed position relative to the prey. As
the actual attack commences, the squid opens its arms over a period ranging from one to
four video frames (33 msec/frame) and then swiftly jets forward at the prey item. An
attack ends successfully when the squid snaps its arms shut, having captured the prey, or,
unsuccessfully when the copepod responds to the attack with a quick escape response and
eludes the squid. This strategy, the first type of attack observed in the youngest squid,
appears to be the most general strategy. Squid utilized this strategy to attack not only
copepods, but also Artemia and other prey species.
Attacks on all species were attempted from all directions, but a preferred direction
of attacks on copepods appeared to be head-on, i.e. towards the anterior head region of the
copepod. This tendency was revealed by a variation in the basic attack that can be
described as "circling" behavior (Fig. 3), in which a squid pursuing a copepod would
move angularly, rotating around the copepod and apparently trying to attain the head-on
position. During this process, the copepod often would react to the squid's approach by
jumping forward at an angle, propelling it out of the squid's lane of approach. In
response, the squid would approach the copepod and repeat the rotation behavior in
another attempt to position itself in front of the copepod. This sequence of action and
reaction often repeated itself many times. Such movements would appear to be an
adaptive behavior by the squid, because the head-on positioning lends to the copepod
jumping partially towards the attacking squid in a fairly stereotyped escape response.
Although the exact direction taken by the copepod may be unpredictable, the possibilities
are basically limited to a solid angle in which the squid is waiting. This would greatly
increase the probability of interception, and circling behavior clearly plays an important
role in the more developed attack strategies discussed below.
In general, the basic attack strategy appeared most successful when the squid
lunged at the copepod from a modest distance with adequate speed. Attacks from
distances above one mantle length almost always failed, regardless of attack speed. As
shown in Fig. 4, essentially all of the filmed successful attacks (days 15-42) occur within
a range of less than 1.0 ML distance. Data in Fig. 4 also show that peak attack speed is
strongly correlated to total attack distance. Thus, very fast attacks are not launched from
short distances. Squid of each age group initiate successful captures over a wide range of
distances, but, as described below, some specialized strategies develop that facilitate
successful captures from both short and long distances.
As Figs. 5A-C show, the correlation between peak attack speed and attack distance
exists in both successful attacks and unsuccessful attempts at all times in this study. The
strength of the correlation appears to increase somewhat with age; however, a quantitative
analysis has not been carried out.
Figures 6A-C show, for each age group, histograms of successful copepod captures
grouped by distance (Group two squid). In Fig. 6A, successful captures in the youngest
squid (days 15-23) occurred from shorter distances, between 0.1 and 0.4 ML. Such
captures occurred when the squid attacked the copepod from a short distance, using an
adequate amount of thrust. During this earlier time period, the squid employed
predominantly the basic attack strategy described above.
As shown in Fig. 6B, day 26 to day 35 squid captured copepods more successfully
throughout a broader range of distances and speeds. While the captures in the lower
range can be attributed to the basic attack strategy observed in the younger squid, the
striking increase in captures from greater distances may be due to a newly developed
behavior. The appearance of these long range captures coincides with the appearance of a
specialized attack strategy to be discussed later, the "arm-intercept.'
In the oldest squid, days 41-42, successful captures were concentrated below 0.4
ML distance, although some still occurred at greater distances (Fig. 6C), and probably
involved arm-intercepts. The apparent improvement in short-distance attack performance
in these oldest squid may be attributed to the development of yet another strategy to be
discussed later, the "tentacular grab." The development of new strategies such as the arm-
intercept and the tentacular grab may allow the squid to explore greater ranges of attack
distances (and speed).
Figures 7A-C show complementary data for unsuccessful attempts by squid of each
age group. In each case, the attack distance distributions for unsuccessful attacks is
skewed towards long distances in comparison with data in Figs. 6A-C, but differences in
the three unsuccessful distributions also exist. The youngest squid in the study appear to
attack from two distance ranges, the primary one below 1.0 ML and a secondary one
above 1.2 ML (Fig. 7A). Squid in the intermediate age group also display attacks in the
same range below 1.0 ML (Fig. 7B). Attacks from greater distances were not observed.
Older, day 42 squid (Fig. 7C) similarly show a similar distribution of attempts
predominantly below 1.0 ML.
Specialized Strategies:
Squid utilize characteristically different attacks at different ages. Speed
adjustments alone cannot account for the changing patterns of attack distance distribution;
rather, these changing patterns reflect the development of specific prey capture strategies
in squid. Here we present two such strategies.
In the intermediate-aged and in the oldest squid, two specific attack strategies were
observed: the arm-intercept and the tentacular grab. In the arm-intercept, (Fig. 8), the
squid first positions itself in front of the copepod, most often through the circling behavior
described above. Having postured itself head-on to the copepod, the squid then opens its
arms up very wide. Next, keeping its arms wide open, the squid jets at the copepod,
The strong jet of the squid triggers the copepod's escape response and the copepod
projects forward at some angle. Because the squid's arms are wide open, the copepod
may, during its escape attempt, run into the squid's arms to be captured
A distance/speed plot of attacks unambiguous arm-intercepts reveals that such
attacks usually occur from relatively large distances and speeds. (20.6 ML distance and -
0.3 ML/frame speed). Successful arm intercepts were first observed on day 29 and occur
in both the intermediate and the oldest squid groups, but their earliest developmental
10
appearance is not precisely known.
In the tentacular grab (Fig. 9), the squid must first smoothly maneuver itself quite
close to the copepod (so as not to trigger the copepod’s escape response). When it is in
position, the squid rapidly extends it long feeding tentacles (appendages longer than the
arms) within one to two video frames (33 msec/frame), grabs the prey, retracts the
tentacles, and then wrestles the copepod into submission with its arms. During this
procedure, most of the movement occurs in the tentacles--the body moves only slightly.
Most tentacular grabs occur within 0.4 ML distance and below 0.2 ML/frame speed.
Tentacular grab attempts were first observed in intermediate-aged squid, but successful
captures using this strategy were not observed until days 41 and 42.
Copepod Capture by Artemia-raised Squid:
Results described thus far were obtained on squid that had been exposed to
copepods as the predominant food source from birth, and mortality in this group was
extremely low from day 40 until the end of the study (day 53) as indicated in Fig. 1. On
the other hand, Group three squid were reared from birth on only enriched Artem ia nauplii
and subjected to a complete switch to copepod prey items on day 40. Coinciding with
this switch to plankton, the death count accelerated to more than 30 mortalities per day.
Of the 142 squid present on day 40, only six survived to day 53.
During the period of copepod exposure, the Group three squid clearly recognized
the copepods as potential prey items and made large numbers of attacks. These attacks
were studied on days 41-43 and found to be launched almost exclusively from distances
greater than 0.5 ML (Fig. 10) at speeds appropriate for this range (data not illus.).
11
Despite this, the physical attack sequence differed from that of the plankton reared squid,
however, and very few attacks were successful. When faced with copepods, Group three
squid did not appear to carefully position themselves before attacking or to engage in
normal circling behavior to achieve the head-on position. Comparison of Fig. 10 with
Fig. 7C indicates that the distribution of unsuccessful attack distances in Group three
squid is skewed towards long distances relative to those of the equivalent age group of
plankton-fed Group two squid. Moreover, Group three squid showed no attempts
whatsoever from the close (short distance) range below 0.4 ML, over which the day 42
Group two squid were highly successful. Instead, the 41-43 day old Artemia-raised squid
are more similar to the youngest group two squid studied (15-21 days) in that both
displayed a high percentage of long-distance failures (Fig. 10 vs. Fig. 7A).
V. Discussion:
In this discussion, two points shall be addressed: first, copepod capture is an
ability that must be acquired through experience; and second, squid acquire such an ability
through a progressive development of increasingly complex strategies.
Acquisition of Prey Capture Behavior-A Window of Opportunity:
Proof that experience is critical in the ontogeny of copepod capture is most evident
in a comparison of mortality counts between group two and group three squid. Before we
develop this point, let us first interpret the mortality data. As food type was the only
variable manipulated in the comparison between group two and group three squid,
significant differences in mortality between the two groups can be attributed to diet-
12
dependent factors. All other factors, environmental and handling factors included, were
identical in the two groups. Invariably, "noise" in the mortality records emerges during
such an experiment that makes detailed comparisons between groups difficult, and
replicate experiments can help separate "signal" from noise. Results of the prey-item
switch described in this report were confirmed in a previous experiment carried out one
year earlier.
Before squid can acquire specific strategies for copepod attacks, they must possess
the basic ability to attack and feed during the first 1-2 weeks of life. The initial wave of
mortality between day one and day 13 in both Groups two and three most likely is due to
squid that perished from starvation because they did not make the transition from internal
yolk nourishment to feeding by developing successful prey capture (Hanlon & Hixon,
1983). Thus, those squid that survived the first mortality wave must possess the
fundamental attack skills described in this paper as the "basic attack." We are presently
studying this two-week period in order to reveal the progression of development of this
behavior necessary for survival.
After the initial wave of mortalities, the subsequent period of low mortality in both
tanks indicates that nearly all the squid were capturing and feeding upon prey. Between
days 26 and 39, Group two squid experienced another wave of mortalities, possibly due to
a change in the feeding regimen. Because of increased copepod availability starting on
day 20, these squid were fed copepods exclusively for 11 days. It is possible that certain
Group two squid had not developed the ability to catch the fast copepods and had been
surviving on the regular provisions of Artemia nauplii during the first 20 days. Faced
13
with an extended period of time where copepods were the predominant, if not exclusive
prey item available in the tank, these squid may have perished from malnourishment.
This explanation would be consistent with the interpretation, to be discussed below, of the
extremely high mortality experienced by Group three squid after the introduction of a
copepod diet. After day 39, Group two squid exhibited minimal deaths until day 53 when
the study was terminated.
An indication of the importance of experience in mastering prey capture is evident
in the mortality data for Group three squid. The dramatic increase in mortality rates that
occurred after the switch to a copepod food source can be attributed to an inability to
catch copepods rather than to lack of prey recognition, as evidenced by the many failed
attempts (Fig. 10). Total mortality during this period vastly exceeded not only that of
Group two during the same time period (days 41-52), but also that suffered by either
Group two or three squid during their initial introduction to prey directly after hatching.
These comparisons suggest that after 40 days, the squid's ability to master copepod
capture is greatly impaired.
We hypothesize that squid deprived of exposure to their natural food source of
copepods for several weeks after birth fail to receive the developmental cues and
experience necessary for the ontogeny of copepod capture. Copepod capture is an ability
that must be experientially acquired within the first forty days, more likely earlier than
later. The low rate of survival after switching foods refutes the idea that copepod capture
may be simply an innate ability or a developmentally programmed skill. An additional
strong indication that copepod capture is an acquired ability can be found in the
14
improvements in capture frequency and refinements in technique between younger and
older Group two squid.
Analysis of Group three squid attacks on copepods (days 41-43) reveals that these
squid resemble younger (day 15-23), Group two squid in their fast, long distance attacks.
While such long distance attacks were not observed in Group two squid after day 26, they
predominate in Group three squid at day 41. Long distance attack attempts probably
reflect either a lack of agility that prohibits a close approach of the copepod without
triggering its escape response, or the inability to properly time reactions to the erratic, fast
moving prey. Thus, these older, but inexperienced squid appear to be developmentally
stunted at a level more or less similar to that of Group two, day 15-23 squid exposed to
copepods shortly after hatching.
Exceptions do occur. Out of the 142 Group three squid alive on day 40 when
copepods were introduced, six had survived the crash 12 days later. Presumably these
squid possessed the ability to catch copepods. Despite the lack of exposure to copepods,
these six may have developed such an ability independently, by some mechanism other
than experience with copepod attacks, or they may have been extraordinarily flexible in
their ability to acquire the new skills necessary for copepod capture at day 40.
Progression of Strategies During the Period of Acquisition:
Having established that copepod capture is an acquired ability, we now move on to
examine the progressive development of this ability. First, the correlation between attack
distance and peak attack speed strongly suggests that a squid can accurately gauge the
distance between itself and the prey target, and then adjust its attack speed accordingly.
15
Such a correlation roughly forms a 45 degree line as shown in Fig. 4. Points significantly
below this 45 degree line are indicative of a slow approach that would not be expected to
be successful unless coupled to a special strategy, such as the tentacular grab. The
paucity of points above this line implies that squid can accurately adjust attack speed to
match attack distance, and that they do not use more speed than is necessary. The fact
that a correlation exists in successful and unsuccessful attempts at all age groups studied
indicates that the ability to gauge distance and adjust attack speed accordingly either is
inborn or develops before day 15. Careful observation of the earliest feeding attempts by
squid on copepods would serve to distinguish these possibilities and to reveal the
ontogeny of the basic attack pattern. This work is presently in progress.
For the youngest squid in the study (days 15 to 23), the dominant strategy was the
basic attack. Although the successes only appeared to occur when the squid attacked from
short distances using sufficient speeds, many squid still attacked from above 1.0 ML, a
distance beyond which no successful captures were observed. The almost complete
disappearance by day 26 of attacks in this ineffective, long distance range takes on a
developmental significance as a means by which squid apparently improve their chances
of copepod capture. Such long, futile attacks were apparently selected against. Whether
the squid displaying these attacks died or modified their behaviors is not clear.
During days 26-35, squid expanded their effective attack range through the use of a
new, specialized attack strategy. The regular appearance of successful captures originating
from above 0.5 ML distance marks this development, and the appearance of the bimodal
distribution evident in Fig. 6B is consistent with the idea that squid in this age group
16
employed more than one strategy. The basic attack strategy most likely accounts for the
captures at distances less than 0.4 ML, whereas the more recently acquired arm-intercept
at least partially accounts for the improved performance in the longer distance range.
Arm intercepts, which were still practiced by day 41-42 squid, largely account for
the existence of captures at greater distances in the oldest squid studied, but in this group,
successful attacks were most prominent in a region of very short distances and low
speeds. Coinciding with this shift in attack parameters is the first appearance of
successful tentacular grabs (day 41), which may serve to allow squid to capture copepods
with less effort, shooting their tentacles out rather than propelling their whole bodies,
This pattern is very similar to that employed by adult squid (Kier, 1982). It is noteworthy
that in the tentacular-based short distance attacks observed in day 41-42 squid, these
animals achieve significantly slower peak attack speeds than do younger squid. It is likely
that such slow attacks require far less energy expenditure than high speed alternatives, but
the extent of savings in relation to the total metabolic requirements of the growing squid
remains to be determined.
Because of significant growth of animals during the course this study,
measurements of attack distance and speed relative to mantle length are obviously
dependent on the size of the attacking squid. As a significant size variation exists within
age groups, and because neither individual nor mean lengths were determined for animals
in either group, the effects of mantle size on the analyses presented here cannot be
rigorously assessed. One might argue that if attack distances and speeds were plotted on
absolute scales, the apparent shifts in the character of attacks between age groups would
disappear. Several points argue against this scenario, however.
First, in comparing successful attacks between the youngest squid and the
intermediate-aged squid, the use of absolute scales would further accentuate the
differences in successful attack character evident in Figs. 6A and 6B due to the more
successful exploitation of a long distance strategy by the larger, intermediate-aged squid
Similarly, absolute comparisons of successes between intermediate-aged and the oldest
squid could be argued to lead to a convergence of attack distances in the histograms
presented in Figs. 6B and 60. However, the shapes of the histograms for these two
groups appear to be decidedly different, and a simple adjustment of the curves by a
constant factor to compensate for average growth would not render the two histograms
equivalent. Finally, unique specialized capture strategies observed to emerge in specific
age groups can account for improved performance at the appropriate distance and serve to
distinguish each age group from the others. The arm-intercept technique that allows squid
to capture copepods from greater distances first appeared in day 29 squid and coincided
with the increase in successful long distance attacks in the intermediate-aged squid.
Similarly, the oldest squid (day 41-42)--the only age group to display the low distance,
low speed tentacular grab strategy--exhibited more successful attacks at shorter distances
The observation of these characteristically unique attack strategies occurring in the two
age groups opposes the argument that attacks by the intermediate-aged and by the oldest
squid differ only relative to the attacking squid's mantle length.
Juvenile squid raised on copepods demonstrate a progressive development of
complex, acquired prey capture behaviors. Squid raised on Artemia nauplii and then
18
switched to a copepod diet demonstrate a lack of such acquired abilities, as evidenced by
a severe mortality rate after the switch.
When considering the results of this study, one must keep in mind that copepods
are but one of many potential prey species in the wild. While this study may provide
insight into development in the field, the complete picture is surely much more complex
as juvenile squid most likely feed on a multitude of species and may have specific
strategies for each species. Just as Artemia fed squid appear handicapped in prey capture
ability when introduced to copepods, the relatively competent squid raised on copepods
may likewise be impaired if they were to be introduced to the wild. Such knowledge
would be important if, in the future, squid reared in tanks were released into the wild, for
tracking studies or for attempts at repopulation, for example. For mariculture, results of
this study reflect on the advisability of certain abrupt changes in feeding regimen,
Neurobiologist may be able to capitalize on behaviorally impaired organisms, such as the
Group three squid, to search for neurological signs of the behavioral deficit in these
organisms. Finally, the notion of experience-based modules of behavioral development
may be a factor to consider in designing neurobiological experiments.
Acknowledgements:
We would especially like to thank Gilbert Van Dykhuizen and the Monterey Bay
Aquarium for their assistance and the use of their facilities in rearing the squid, and for
their valuable input into this study.
19
VI. Figure Legends:
Figure 1. Daily Mortality Count. This chart details the mortalities in Group two and
Group three squid. The feeding regimen for both groups of squid is indicated by
the horizontal bars directly beneath the X-axis. Note the dramatic increase in
mortality in Group three after the switch to a copepod diet on day 40.
Figure 2. The Basic Attack Sequence. Squid utilized this most general strategy, the first
to be observed in the youngest squid, in attacks on both copepods and Artemia
nauplii.
Figure 3. "Circling" Behavior. Before lunging at the prey item, squid often maneuvered
angularly to obtain position in front of the copepod prey. As the squid
repositioned itself in response to the copepod's escapes, its overall motion appeared
circular.
Figuie 4. Successful Copepod Attacks Grouped by Age. This scatter plot shows the
distribution of successful copepod captures by Group two squid along axes of total
attack distance and peak attack speed. Note the correlation between total attack
distance and peak attack speed, as revealed by the distribution of points along the
45 degree line.
Figure 5A. Successful and Unsuccessful Attacks by the Youngest Squid.
5B. Successful and Unsuccessful Attacks by the Intermediate-Aged Squid.
5C. Successful and Unsuccessful Attacks by the Oldest Squid.
A comparison of these scatter plots reveals that, with age, the distribution of
attacks on copepods is shifted towards shorter distances and lower speeds. Note,
once again, the apparent correlation between attack distance and attack speed in
both successful and unsuccessful attacks.
Figure 6A. Successful Captures, Group 2, Days 15-23.
6B. Successful Captures, Group 2, Days 26-35.
6C. Successful Captures, Group 2, Days 41-42.
These histograms of successful captures reflect the changing character of successful
copepod captures. Refinements in strategy allow the intermediate-aged squid to
expand their effective copepod capture range, and also facilitate captures by the
oldest squid from shorter distances.
Figure 7A. Unsuccessful Attacks, Group 2, Days 15-21.
7B. Unsuccessful Attacks, Group 2, Day 33.
7C. Unsuccessful Attacks, Group 2, Day 42.
These histograms depict the attack distance distributions in unsuccessful attacks.
The upper range of attack distances present in days 15-21 squid has almost
completely disappeared in the older squid.
20
Figure 8. The Arm-Intercept. First observed in day 29 squid, this strategy allows squid
to capture copepods from greater distances.
Figure 9. The Tentacular Grab. A low distance, low speed attack strategy, the tentacular
grab, observed in day 41-42 squid, may facilitate copepod captures at reduced
energy expenditures.
Figure 10. Attacks on Copepods, Group 3, Days 41-43. The presence of ineffectual, long
distance attacks in these Artemia-raised squid, and the similarity in attack distance
distribution between these and the younger, day 15-21 squid (Fig. 7A) may reflect
developmentally impaired prey capture abilities that resulted from a lack of
exposure to fast moving copepod prey early in life.
21
VII. References Cited:
Hanlon, R.T. and Hixon, R.F., 1983. Laboratory maintenance and culture of octopuses
and Loliginid squids in Culture of Marine Invertebrates, C.J. Berg, Jr., ed.,
Hutchinson Ross, Stroudsburg, Penn, pp. 44-61.
Hurley, A.C., 1976. Feeding behavior, food consumption, growth, and respiration of the
squid Loligo opalescens raised in the laboratory. Fisheries Bulletin, 74(1): 176-
182.
Kier, W.M., 1982. The functional morphology of the musculature of squid (Loliginidae)
arms and tentacles. Journal of Morphology, 172: 179-192.
Yen, J. and Fields, D.M., 1992. Escape responses of Acartia hudsonica (Copepoda)
nauplii from the flow field of Temora longicornis (Copepoda). Arch. Hydrobiol.
Beih., 36: 123-134.
22
29
09
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92




—

8



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54
5582
JOE
The Basic Attack Sequence

(1) Squid postures
at copepod
(3) Arms open
wider

(5) Arms close:
squid catches copepod
Fig. 2

(2) Arms begin
to open
(4) Squid lunges
at copepod
"Circling" Behavior
(1) Squid moves to
achieve position
in front of copepod
(3) Squid moves laterally
to regain position in
front of copepod
S

L
9
(2) Copepod
leaps away
(4) Copepod jumps
to new position
(6) Copepod moves
(8) Copepod moves


(9) Squid reacts, etc.

Fig. 3
(5) Squid once again
maneuvers in front
of copepod
(7) Squid reacts
S
.
89
8
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9



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X X
X X
X
XX

X( XX
XX
X
X X
X


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.
T 0
5 0
—

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XX








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—
X
X

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8
eny
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Successful Captures, Group 2, Days 15-23




C
-
k taava-
Attack Distance (ML)
Figure 64
Successful Captures, Group 2, Days 26-35
9



O
—
8 8
Attack Distance (ML)
Figure 6B
10
4
0
Successful Captures, Group 2, Days 41-42

a taatai

8
Attack Distance (ML)

Figure 60
Unsuccessful Attacks, Group 2, Days 15-21
20
18
14
5 10
O
L
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addaadad--------
aaaa
Attack Distance (ML)
Figure 74
20
14
Unsuccessful Attacks, Group 2, Day 33
N


oooo--ooo-oonooo
- - ------addodooi
ooooooo
Attack Distance (ML)
Figure
20
Unsuccessful Attacks, Group 2, Day 42

0
ooo--oood-oonooo
— — — — — — — — —
oooodoo
o v di di di di di di oi
Attack Distance (ML)
Figure 70
The Tentacular Grab

5






Fig. 8
(1) Squid postures near copepod
(2) Squid arms begin to open
(3) Squid arms open;
tentacles begin to extend
(4) Tentacles fully extend and grab copepod
(5) Tentacles retract;
copepod captured
The Arm-Intercept
Fig. 9


(1) Squid circles to achieve position in front of copepod
(2) Squid arms begin to open
S


(3) Arms open wide

(4) Squid lunges (a),
copepod makes escape attempt (b)
but runs into squid's arms
(5) Squid grabs copepod-successful capture
Figure 10
Attacks on Copepods, Group 3, Days 41-43
20
18
Note: All attacks were
unsuccessful
5 10


ooo--oood-ooooo
—————— — ——
oooooo
div oi ddoicioioi
Attack Distance (ML)