(Christian
Albrechts Universität Kiel)
RUTGERS UNIVERSITY
(accepted April 23 1992 - Arch Hydrobiol Beih 36: 83-96)
(this publication is a sketch of the technical setup and some recordings of transparent juvenile fish, performed from the ATOLL iceSTATION Laboratories in the Baltic, Kiel, Germany - manuscript for the international meeting @ Lake Lacavac on quantitative imaging and acoustics - invited speaker - mirrored here partially for discussion and teaching purpose only - for citation go to the original printmedia)
The behavior and microdistribution of juvenile
herring Clupea harengus and the copepod Acartia discaudata
have been investigated in Kiel Fjord. For in situ measurements
at high magnifications in real-time, two tools have been developed: the
"ecoSCOPE", an imaging system allowing for an approach close enough to view the evasive
predators as well as their prey via an endoscope, and the "dynIMAGE"
program, an image processing software allowing for compensation of system-vibrations
and microturbulences. The dynamic processes inside of a zooplankton-microlayer
are analyzed at the mm-scale to investigate how small-scale physics affect
feeding success. At microscales the maximum organism-concentrations were several
orders of magnitude higher than derived from conventional net samples. Juvenile
herring (mean length 38 mm) grazed down the copepod patches (up to 850 individuals
per liter) within minutes, attacking each copepod separately. The mean frequency
of this particulate feeding was 2.4 captures per second at the individual
level and up to 84 per liter per second at school level, indicating the extraordinary
grazing success of clupeid predators in micropatches caused by interactions
between ocean physics and biology.
The importance of microdynamics and microdistributions of predator and
prey for the ecology of the early life history of fish has been emphasized
by Lasker (1975, 1988), Vlymen (1977), Steele (1978, 1980), Wroblewski (1984),
Mackas et el. (1985), Rothschild (1986, 1988), Rothschild & Osborn (1988)
and others. Patchiness of prey as well as patchiness of predators - mostly
referred to as schooling - are regarded to be key factors in determining
the successful recruitment of many commercially important pelagic fish species.
The importance and implications of behavioral studies have been demonstrated
by Blaxter & Hempel (1963), Brooks & Dodson (1965), Rosenthal &
Hempel (1970), Blaxter & Staines (1971), Rosenthal & Fonds (1973),
Blaxter (1974), Hunter & Thomas (1974), Hunter (1980), Janssen (1980),
Coughlin & Strickler (1990) and others from laboratory investigations.
Several working groups now apply optical systems in situ (see discussion)
and their results clearly indicate the need for more detailed studies at
microscales with very high resolution in time and space. This paper describes
the function of two tools permitting a closer view of the very complex processes
when highly motile predators encounter extremely alert and evasive prey.
These tools have been developed within a project on the orientation of pelagic
fish in environmental gradients. One objective of the project is to learn
how herring-schools orientate under the changed environmental conditions
of the Baltic: how do they search and encounter their prey under the drastically
reduced visibilities of the enhanced phytoplankton blooms observed
in the Baltic during the
last decade? Some preliminary quantifications of feeding dynamics of
juvenile herring and the escape capacity of their prey are presented and
discussed.
Material and Technology
In an area of the Baltic Sea known to be a major feeding ground for juvenile
spring spawning herring, optical and acoustical in situ systems were
deployed for behavioral studies. During days with moderate wind speeds,
copepods concentrated directly
at the halo- and thermocline below the flume of the Kiel Canal in front
of the locks of Kiel-Holtenau (54.22.05 N, 11.09.05 E). In late summer,
schools of juvenile herring (Clupea harengus, body
lengths between 3.5 to 6 cm) migrate through this area into the open Baltic.
The visibility is generally very poor due to massive plankton blooms. In
this location, the swimming laboratory "ATOLL" (a 27 m doughnut-shaped
structure) is anchored (Kils
1986), allowing for long time monitoring of this process: In front of
underwater observation windows,
optical sensors measure
the microdistribution and the behavior of predators and their prey in relation
to ocean physics and biological gradients. In calm weather conditions, the
copepods concentrated in thin microlayers at a depth of 1.2 meter. For example
copepod concentrations (Acartia discaudata, > 95 % adult females,
some A. bifilosa) increased from less than 1 ind. / l to more than
850 ind. / l over a vertical distance of 30 cm. The vertical extension of
these microlayers was a few decimeters. Although the visibility was very
poor (Secchi depth 1.8 m) juvenile herring schools found these micropatches
within half an hour from the time they first formed, and within minutes they
grazed them down.
The optical and acoustical sensors are deployed from a small remotely operated vehicle (ROV).
Although this ROV is quite small and quiet it was impossible to approach feeding herring
closer than 40 cm (Fig. 1).
From this distance, however, the copepods in front of the herring are invisible
due to the deflection of light
by phytoplankton and microparticles in the highly productive waters
of the western Baltic. By imitating the long and thin snout of the garfish
protruding into the security sphere of the alert herrings (Fig. 1), we designed an endoscope
with a tip diameter of 11 mm. The endoscope is camouflaged to reduce the brightness-contrast
against the background: the top is black and the sides are silvery. Additionally,
the front of the ROV is covered by a mirror, reflecting a light gradient
resembling the natural scene and making the instrument body virtually invisible
to the animals. The "ecoSCOPE" allowed observation of the feeding
herring from a distance of only 4 cm. The predators are illuminated by natural
light, the prey by a light sheet, projected via a second endoscope from strobed
LEDs (2 ms, 100% relative intensity at 700 nm, 53% at 690 nm, 22% at 680
nm, 4% at 660 nm, 0% at 642 nm). A second sensor is imaging other copepods,
phytoplankton and particles at very high magnification (Fig. 1 CCD-array b, Fig. 2 shows the front part
of probably Acartia discaudata). A scanning SONAR-sensor is used to
find the microlayer and the herrings from 40 m distance. Details of the optics
are described in Kils (1989).
Another advantage of these small "optical probes" is the minimal disruption
of the current-field in the measuring volume, allowing for less disturbed
surveys of microturbulence and shear.
The signals from the scanned images are transferred to the memory of the
board-unit (three Motorola 68000, Euro-bus/VME, 8 Mhz, 12 Mbyte RAM) for
storage and evaluation. During the measurements the images can be observed
in false colors in real time, strobed or frozen. The last six seconds can
be played back on demand from memory. This direct observation can serve only
for a first rough detection and estimation of high organism concentrations
because the images pass too fast for the human eye when three coordinate-systems
are constantly moving: the optical system vibrates, the objects move, and
the water is turbulent in mm- and dm-scales. This prohibits a direct evaluation
of the camera signals by the human eye, especially at high magnifications
which result in considerable angular speeds of light from the focused objects.
For further analysis, the software package "dynIMAGE" has been developed:
After a measurement, the processing system displays the image-sequence of
an attacking herring frame by frame to the operator. In the raw image-data,
a quietly hovering prey or a stationary floating particle shows up on every
frame at quite different locations, because the optical system has moved
in the time elapsed between frames due to microturbulences in the dm-range
accelerating the ROV. Such a hovering particle is marked by the operator
with a cross-hair-cursor driven by a track-ball at one of the frames as a
reference as well as on the frames before and after. The derived x,y coordinates
are used by the program to shift all images to the first reference point,
correspondingly. In this new film, the system vibrations are filtered out:
the marked hovering particle is displayed stationary now and the eye can
concentrate better upon the prey, the approaching predator and the remaining
microturbulence-field.
Optionally each frame can be contrast-enhanced, changed in brightness and
cleared from background-distortions and noise before the system recalculates
the animation. This "shifted" scene can be played back on the board unit
already in real-time or slow-motion, forward and reverse.
Alternatively dynIMAGE can synchronize the animation to the movements of
the operator`s hand: moving the mouse to the right switches frames forward,
moving to the left backwards. This tool serves as an interface to the image
processing capabilities of the human eye and brain for a better interpretation
of the fast dynamics by focusing the interest on any detail of the scene
at optimal replay-speed.
If other particles adjacent to the marked particle now show up more or
less stationary too, the selection was all right; if not, the reference-particle
had its own propulsion - like a swimming zooplankton - so a new reference
point should be selected.
Subroutines interactively calculate distances between particles, sizes
of the organisms, areas, vectors of movements, angles between organisms,
contrasts against the background, velocities of predator and prey and water
velocity-shear by tracking algal cells or detritus. In the image-processing,
markers can be left behind on the monitor for tracking and counting of organism
frequencies. The results, the coordinates and the tracks can be stored as
LOTUS 123-, ASCII- and TIFF-image files for export to MS-DOS systems. The
processed animations are stored on magneto-optical disks. The images can
be transferred to other computer systems for further evaluation (Meta-, TIFF-
or EPS-format on IBM, Macintosh, NeXT or VAX). The animations can also be
transformed to a standard video signal for tape recording (RGB or composite
video in PAL or NTSC, 50 or 60 hz).
With respect to memory requirements and high processing speed a resolution
of the images of 320 times 200 pixels at 16 intensity levels was selected
for the behavioral analysis (DELTA and JPEC compression routines additionally
reduce each 32 kilobyte images to approximately 2 - 25 kilobytes). This
relatively low resolution is a fair compromise for evaluation of dynamic
processes, considering that an animated sequence appears to the human eye
much sharper than the single frames do. Due to the deflection of the light
by phytoplankton, in the plankton-rich waters of the Baltic the sharpness
of in situ images is not much higher anyway. For applications which do not
need the full 50 frames per sec images can be scanned at 640 times 400 pixels
in true colors (the CCD-chips have 440 000 pixels).
It will be only a mater of time
until portable computer systems will be available to handle the high resolution
in real-time.
Fig. 2 shows an image of the prey-sensor
(see Fig. 1 CCD-array b), probably Acartia discaudata.
Fig. 3a shows an image of the predator-sensor (see Fig. 1 CCD-array a),
it is image no. 21 of an animation as delivered by the system printer. The
image shows the encounter of a copepod (marked as A, probably Acartia discaudata)
and an approaching juvenile herring. The copepod is escaping at a speed of
more than 72 mm per second over a distance of more than 8 mm. At the end
of this escape reaction it tumbles for about 440 ms. However, the predator
does not attack this staggering copepod directly in front of his mouth but
is aiming at another one (Fig. 3b copepod B) more than 10 mm above his eyes.
Another 160 ms later the herring is catching copepod B from below by opening
the mouth (Fig. 3c) and 40 ms later spreading the opercula (Fig. 3d). The
fish then returns to its horizontal position (Fig. 3e). In Fig. 4, the outlines
of the silhouettes of the head of the approaching predator are drawn in a
time-series (40 ms intervals) derived from images no. 17 to no. 22 indicating
the high escape speed and the tumbling. The following milliseconds are drawn
in Fig. 5 (images no. 23 to no. 30). Fig. 6 shows the velocities of the escaping
copepod A and the results of the evaluation of another animation (C). In
the first few seconds after the school detected the microlayer the average
frequency of this particulate feeding was 2.4 per second (for a single fish).
Four to six attacks could
be observed in succession, as demonstrated in the time-series of Fig. 7. During
this process, the predators come higher and higher in the water column due
to the oblique attack direction. After swimming down without feeding at
an angle between 40 to 70 degrees and a speed of 4 to 6 body lengths per
second the herring immediately start a new feeding sequence.
With the help of an endoscope and high speed macro optics, it is possible
to approach a feeding school of juvenile herring close enough to roughly
image their prey as well. The dynamics inside such feeding assemblages are
fast and complex. By "shifting" single images the system vibrations are compensated
for a "filtered" playback of the processes to the human eye. This facilitates
a better analysis of predator/prey interactions. The use of an LED light sheet
permits imaging of transparent copepods and a rough quantification of prey-abundances
as well as swimming distances, speeds and directions. Although the light
of the LEDs is visible to the human eye, no noticeable responses of herring
or copepods could be observed when they entered the light sheet alone. For
herring the optimal sensitivity is around 510 nm with a minimal response
at 660 nm (Blaxter 1964). At 660 nm the LEDs produce only 4% of the radiation
emitted at 700 nm.
Herring predation act can be broken up as described for other species by
Holling (1959), Gerritsen & Strickler (1977) and O'Brien (1979) into
a series of discrete components: location, pursuit, attack and capture. The
attack is directed upwards corresponding with the laboratory findings of
Blaxter & Holliday (1958), Janssen (1978), Batty et al. (1990) and Gibson
& Ezzi (1990). The observed mean frequency of 2.4 ingestions per second
for a single fish is comparable to frequencies (1.9 - 2.3) found by Janssen
(1976) for particulate feeding by Alosa pseudoharengus at high prey
concentrations in the laboratory. The ram-jaw feeding mechanism of herring
on a copepod is very similar to the blue-green puller fish Chromis viridis
feeding on Eucalanus crassus as described by Caughlin & Strickler
(1990), although in herring the process is considerably slower. The protrusion/retraction
time for C. harengus is 40 to 80 msec which is close to the 30 to
60 msec Motta (1984) found for Chaetodon miliaris and in the range
of 40 - 100 msec given for ten species by Motta (1988).
The wide opening and protrusion of the mouthparts as well as the steady
position of the attacked copepods indicate that the herring uses little suction
to avoid shear which would alert the prey (Janssen 1976, 1978; Drenner et
el. 1978; O'Brien 1979; Launder 1980; Liem 1980; Launder & Liem 1981;
Vinyard 1982; Wright & O'Brien 1984; Kettle & O'Brien 1987; Yen 1988).
As indicated in Fig. 3 d, C. harengus did not seal its opercular cavities
but spread out the opercula, possibly to allow water to flow out as water
moves in the protruding mouth surrounding the prey. The observed escape speeds
of A. discaudata (60 - 72 mm per second, flight distance 8 mm, body
length = 0.8 mm) are similar to those reported for A. fossae (65 -
90 mm per second, flight distance 8 mm, body length = 0.7 mm) by Yen (1988),
Cyclops strenuus (34 - 49 mm per second, body length = 0.6 mm) by Rosenthal
(1972), and Cyclops scutifer (69 - 85 mm per second, body length =
1.5 mm) by Strickler (1975), but slower than those reported for Diaptomus
sp. (132 mm per second, body length = 1 mm) and Cyclops scutifer
(272 mm per second, body length = 0.7 mm) by Strickler (1977) or for the
bigger Calanus finmarchicus (161 - 369 mm per second, flight distance
12 - 18 mm, body length = 2.2 mm) by Haury et al. (1980). The described successful
escape of copepod A in Fig.4 indicates that a darting of 72 mm per second
can be sufficient for a 0.8 mm copepod to escape from an attack of a 38 mm
juvenile herring and portrays them as highly evasive prey as discussed by
Singarajah (1969, 1975), Confer & Blades (1975), Swift & Fedorenko
(1975), Drenner et al. (1978), O'Brien (1979), Drenner & McComas (1980),
Haury et al. (1980), Kerfoot et al. (1980) and Vinyard (1982).
These preliminary and rough results indicate an extraordinary grazing success
of clupeid predators when the random distribution of copepods is altered
by ocean physics. Such extreme prey concentrations occur with a somewhat
higher chance in calm weather conditions, at strong stratifications, and
at horizontal edges like convergences or shorelines. Although these patches
are exceptional in time and space, their encounter yields much energy to
cruising schools of juvenile clupeids and should be of considerable importance
for the early life history of pelagic species. From the measurements with
these new tools a theoretical maximum grazing rate of up to 84 particulate
feedings per liter per second at the school level can be estimated.
Denman & Gargett (1983), Sundby (1983), Yamazaki & Osborn (1988),
Costello et al. (1990), Haury et al. (1990), Marasse` et al. (1990), Osborn
et al. (1990), Sundby & Fossum (1990), Yamazaki & Kamykowski (1991)
and Donaghay & Sieburth (1992) clearly show the biological importance
of structures and dynamics in the mm- and msec-scales. More effort should
be invested in further developments of imaging systems as tools for in
situ ecological studies: Besides multi-nets (Wiebe et al. 1976), Longhurst-Hardy-Plankton
Recorders (review by Haury et al. 1976), high frequency acoustics (Holliday
et al. 1989; Smith 1992), optoelectronic counters (Herman & Dauphinee
1980), advanced in situ imaging instruments with high resolution in
time and space like GULF III type plankton samplers with photo- or video-
cod ends (Ortner et al. 1981) and the directly imaging Video Plankton Recorder
(Davis et al. 1992) are needed for detailed descriptions of organism abundance
and distribution. However, as a next step we should also enhance the instruments
capabilities to quantify behavior like the in situ Crittercam, the
ROVs of Bergstrðm et al. (1990) or Marschall (1988), the high
speed in situ cameras of Motta (1988) or Kils (1989), the free-falling in
situ camera with multi-strobes by Kils (1981) or the three-dimensional
video system of Hamner et al. (1988). For a better understanding of microstructures
ethological knowledge can be of great help, because the slightest alteration
in behavior can cause patchiness (Fraenkel & Gunn 1961; Vlymen 1977; Hamner
1988; Price et al. 1988; Ramcharan & Sprules 1989). This research is
envisioned of a developing effort on microscale methods and investigations
which are planned under the umbrella of Global Ocean Ecosystems Dynamics (GLOBEC).
One of the objectives of GLOBEC is the "Concentration of First Principles",
the understanding of how important processes at the level of individual organisms
control population abundance: "Special emphasis needs to be given to assessing
the little-studied roles of ocean physics in feeding success, growth rates,
reproductive output, and mortality rates including losses to predators. In
both the physical and the biological disciplines, extensions of improvements
in sampling from the mesoscale into the fine- and microscale environments
are needed" (Muench 1989).
I thank Thomas Seidel and Helmut Thetmeyer for the software work, Alex
Herman, Tom Osborn, Gus
Paffenhoefer, Dietrich Schnack, Rudi Strickler, Hideka Yamazaki and Jeannette Yen for comments on
the manuscript, ATARI, NeXT and SONY for their friendly sponsoring and cooperation,
the VOLKSWAGEN-FOUNDATION for funding, the DEUTSCHE FORSCHUNGSGEMEINSCHAFT
(DFG) for support, Baudirektor G. Brandenburg and the administration of the
Kiel-Canal.
Institut für Meereskunde & Institut für Toxikologie
Christian Albrechts Universität
Kiel - Deutschland
current address:
Institute of Marine and Coastal
Sciences
RUTGERS, the State University of New Jersey
New Brunswick, New Jersey 08903-0231, POB 231
email kils@imcs.rutgers.edu
update 020130
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