Journal of Plankton Research Vol.18 no.9 pp.1699-1715, 1996
Motion behavior of nauplii and early copepodid stages of marine
planktonic copepods
G.-A.Paffenh6fer, J.R.Strickler1, K.D.Lewis and S-Richman2
Skidaway Institute of Oceanography, 10 Ocean Science Circle, Savannah, GA
31411, 'Center for Great Lakes Research, University of Wisconsin, 600 East
Greenfield Avenue, Milwaukee, WI53204 and 2Department of Biology, Lawrence
University, Appleton, WI 54912, USA
Abstract. The goal of this study was to quantify periods of activity and velocities of late naupliar and
early copepodid stages of planktonic copepods occurring regularly on the southeastern continental
shelf of the USA. We obtained quantitative information on eight species, including adult females of
Oithona plumifera. All studies were conducted at food concentrations near or above satiation levels.
Activities ranged from 0.85% (adult females of O.plumifera) to 100% of time (nauplii and copepodids
of various calanoid species). Motion velocities (excluding escape motion) covered more than one
order of magnitude: from 0.39 mm s~' for nauplii of Temora stylifera to 5.24 mm r 1 for nauplii of
Oncata meditenanea. Ranges of activities of species range from occasional for early juveniles to adult
females of O.plumifera to 100% for the same range of T.stylifera, the latter creating a feeding current
from N i n onwards, the former not at all. Of notable interest is Centropages velificanis which moves
intermittently as a late nauplius, continuously as an early copepodid and intermittently as an adult All
observed calanoid late nauplii and copepodids move in three dimensions, excluding copepodids of the
shelfbreak/oceanic Paracalanus oculeatus. The results indicate not only significant differences in
motion behavior between cyclopoids and calanoids, but also between calanoid species. Yet, some
calanoid species show little ontogenetic changes at all.
Introduction
Marine planktonic copepods are able to displace themselves using their cephalic
and thoracic appendages. The motion of planktonic copepods includes diel vertical migration, ontogenetic migration, escape and relocation motion (jumps), and
undisturbed slow motion which usually falls under the category of 'swimming',
which often alternates with sinking (e.g. Lowndes, 1935). Swimming activities and
velocities of adult calanoid and cyclopoid species have often been studied (e.g.
Storch, 1929; Lowndes, 1935; Gauld, 1966; Strickler, 1977; Shuvayev, 1978; Buskey,
1984; Landry and Fagerness, 1988; Uchima and Hirano, 1988;Tiselius and Jonsson,
1990, Ramcharan and Sprules, 1991). As the copepods propel themselves, they displace water which includes the creation of a feeding current which has been
reported for late copepod stages and adults of various calanoid species (e.g.
Lowndes, 1935; Strickler, 1982) and nauplii of two species (Storch, 1928; Paffenh6fer and Lewis, 1989). A feeding current can reach a velocity of 5-10 times that
of the cruising speed of an adult female and greatly enhances the probability of
encountering a food particle (Strickler, 1985; PaffenhOfer and Lewis, 1990).
In comparison to adults, information on the motion of early juvenile stages of
calanoids and cyclopoids is scarce. The first report on swimming of nauplii of
planktonic copepods was by Storch (1928) on Diaptomus gracilis and Cyclops
strenuus. Gauld (1958) reported on nauplii of Oithona similis and Calanus finmarchicus. The swimming behavior of nauplii of various species was described in
detail by Bjdrnberg (1972, 1986a). Gerritsen (1978) quantified the swimming
© Oxford University Press
1699
G-A.PafTenhofer et al
velocity of various juvenile stages of Cyclops scutifer, as did Buskey (1994) for
Acartia tonsa, and Landry and Eagerness (1988) for nauplii and first copepodid
stages of three calanoid species. The mouthpart activity of Eucalanus pileatus
nauplii and first copepodid stage was determined by Paffenhdfer and Lewis
(1989), and Buskey et al (199.3) determined the velocity of the first naupliar stage
of several calanoid and cyclopoid species. However, despite the fact that'... the
nauplius represents the most abundant type of multicellular animal in existence'
(Fryer, 1986), and that 'even within single major groups there are great differences
in ecology, habits, and abilities ...' (Fryer, 1986), the scientific community has not
paid much attention to early juveniles of planktonic copepods, with occasional
exceptions (e.g. Gauld, 1958; Bjdrnberg, 1972,1986a,b). Since nauplii, despite their
abundance, seem to be more vulnerable to invertebrate predation than early
copepodid stages (e.g. Landry, 1978), and nauplii of different species differ in their
vulnerability to copepod predation (e.g. Paffenhdfer and Knowles, 1980), an
investigation seems to be warranted to determine differences in motion behavior
between nauplii of various abundant copepod species, and between nauplii and
early copepodid stages (Table I).The goals of our study were to quantify (i) which
nauplii and early copepodids created a feeding current, (ii) what percentage of
time they moved actively (i.e. excluding sinking), (iii) how fast they moved, (iv)
what distance was covered per unit time (including active and passive periods)
and (v) how they moved in space. Overall, these observations were intended to
advance our general understanding of the motion behavior of juvenile copepods
before and after their metamorphosis to copepodid stage I.
Method
We investigated six species of calanoids and one cyclopoid species (Table I). All
seven species occur during part of each year on the middle to outer shelf off the
southeastern USA (Bowman, 1971; and personal observation). Some of these
species also occur in other regions of the subtropical to tropical oceans (e.g.
Table L Body (nauplius) and cephalothorax (copepodid) length, stage, presence or absence of a
feeding current of seven species of planktonic copepods, and taxon and concentration of food
Species
Stage
Length (mm)
Centropaga velificatus
NIU-VI
0.20-036
039-O.51
0.71-1.15
037-0.60
0.75-0.89
0.14-0.17
0.18-0.26
032-0.42
0.18-022
0.24-035
0.20-0.28
032-038
ci-n
Eucolunus hyalinus
Eucpioiiw pilffltm
NIV-VI
NIV-VI
Oncaea meditenanea
Paracalanus aculeatus
NIV-V
NIV-VI
ci-n
ci-n
Porocoliinus onosunoiio NV-VI
Temora stylifera
ci-n
NIV-VI
ci-n
Feeding current Algae: taxon and
concentration (mm31~')
0.29-0.45 Rb, 0.6-0.7 Gn
No
Yes
03 Rb, 1.0 Gn
0.8Tw,0.8Ra
No
Yes
0.8Tw,fewRa
Yes
0.7 TV, few Ra
No
0.6Rb,1.0Gn
No
029 TV
Yes
029 Tw
No
0281w
Yes
028 Tw
Yes
0.4-0.6 Rb, 0.4-05 Gn
Yes
0.4Rb,0JGn
N, nauplius; C, copepodid; IV, Thalassiosira wassflogit, Ra, Rhizosolenia alattr, Rb, Rhodomonus
baltiar, Gn, Gymnodinium nelsoni.
1700
Motion of naoptfi and early copepodidi
Gonzalez and Bowman, 1965; Sameoto, 1986). We decided, for each species, to
compare the behavior of late nauplii and early copepodid stages, but also to
include, where available, observations on older stages. All these animals were
reared in our laboratory on the algal species shown (Table I). As far as possible,
we offered during our video observations the same food species (the diatom Thalassiosira weissflogii) at satiating food concentrations. Some species did not thrive
on this species and required flagellates. In two cases, we were not able to observe
copepodid stages (Eucalanus hyalinus and Oncaea mediterranea).
All observations were made at 20°C in darkness. Experimental volumes ranged
from 150 to 8000 ml (Table II). Observations were made with a modified Critter
Cam® (Strickler, 1985) at 830 nm wavelength, mounted on a three-dimensionally
operating stage which allowed us to follow the free-swimming copepods continuously over several minutes to 1 h, recording on S-VHS. Motion analyses were
made with software from Peak Performance, Boulder, CO. Velocity analyses were
only made when animals were moving in the plane of the camera, i.e. remained in
focus during the observational period. Although we observed individual copepods
for several to 60 min, we analyzed velocities for -30-60 s per individual, and activities over periods from <5 to >10 min.
Most of the observations were made in volumes of 150 ml (cuvettes) as this
volume, in comparison to smaller ones, reduced the probability of encountering
surfaces markedly. Larger volumes were chosen for continuously moving copepodid stages to limit encountering of surfaces (e.g. Centropages velificatus and
Temora stylifera). In two cases (nauplii of Cvelificatus and T.stylifera), larger
volumes had been chosen because eventually predation experiments with adult
females were to be conducted in the same vessels.
Results
General comparison
Recordings of individual copepods lasted from several to up to 60 min, the latter
being particularly important in detecting occasional brief changes in behavior of
Table H. Species, stage, date and vessel volume of video observations on copepod motion
Species
Stage
Date
Volume (ml)
Cvelificatus
NDI-VI
24 Sept 1992
12 Nov. 1992
30 April 1991
12 Sept 1991
18/20 Sept 1991
27 Nov. 1991
3 Dec 1991
10 Nov. 1992
21 Jan. 1994
21 Jan. 1994
1 Feb. 1994
1 Feb. 1994
30 Sept 1992
28 July-3 Aug. 1994
3000
1000
150
150
150
150
150
150
1000
1000
150
150
8000
1000
ELhyatinus
E.pileatus
ci-n
NIV-VI
NIV-VI
ci-n
O.mediterranea
P.aculeatus
NIV-V
NIV-VI
P.quasimodo
NV-VT
Tjtytifera
NIV-VI
ci-n
ci-n
ci-n
1701
G.-A-Paffenhdfer a aL
intermittently moving stages. One of the significant variables concerning motion
was the presence or absence of a feeding current (Table I). Nauplii and copepodid stages of certain species produce a feeding current (T.stylifera, E.pileatus; also
T.turbinata, not shown). Others, like Paracalanus aculeatus,P.quasimodo and Centropages velificatus, create only a feeding current from copepodid stage I (C I)
onwards. Eucalanus hyalinus is in the same category (CI/II not shown).These data
indicate that even within a genus there can be differences in the motion behavior
of identical stages.
Motion activity
We observed between four and 12 individuals of each group to determine the
percentage of time during which they were actively moving, excluding sinking
(Table III). Here animals are grouped in the sequence of activity. Late nauplii of
five of the seven species studied were moving continuously, including those of
T.turbinata (not shown). Motion of the late nauplii of E.pileatus could be
described as a smooth glide, not moving their Al (first antennae) at all (BjOrnberg, 1986a).Those of T.stylifera also displaced themselves rather evenly, but less
so than those of E.pileatus, and moved their Al in a rhythm with the A2 (second
antennae) and Md (Mandibles). Nauplii of Paracalanus advanced rhythmically
with a gentle hop-like motion (also moving their Al), as did those of E.hyalinus.
Their Al moved slightly in a rhythm with the A2 and Md. Eucalanus hyalinus
often came to very brief stops of a fraction of a second which we did not register
as breaks. In sharp contrast, nauplii of C.velificatus and O.mediterranea were
moving intermittently, the former every 5-20 s, and the latter once, occasionally
twice per minute, making a single leap. Early copepodid activity ranged from
52.5% for E.pileatus to 100% or close to it for the other calanoid species. A statistical comparison [Kruskal-Wallis, and multiple comparison test (Conover,
1980)] of all groups studied reveals no significant differences between adjacent
groups (e.g. O.mediterranea N = Cvelificatus N, but O.mediterranea N * E.pileatus C), but differences from those once or more removed excluding the 100%
active groups. Qearly, the majority of the calanoids studies were always or almost
always moving.
Table HL Percent of time during which late nauplii and early copepodid stages of six calanoid and
one cyclopoid species were moving
X
n
SE
Range
Temora
stylifera
Eucalanus
hyalinus
Eucalanus Paracalanus Paracalanus Centropages Oncaea
velificatus
mediterranea
pileatus
quasimodo
aculcotus
N
C
N
N
100
4
0
100
6
0
100
12
0
100 515 100 97.6
5 5
4 4
0 ±6.9
0 ±Z0
- 42-79 - 92-100
C
N
C
C
C
N
100
7
0
-
91.8
5
±2J
86-98
8^
100 15
8
7 11
±L5
0 ±034
3.4-17.6 - 08-4.7
N, nauplius; C, copepodid; £, mean; n, number of animals observed; SE, standard error.
1702
N
N
Motion of nanpUi ind early copepodids
Velocity and distance traveled
We determined the motion velocity (excluding sinking) of 4-12 specimens of the
previously mentioned stages and species, and present the results in the sequence
of decreasing velocity (Table IV): those which moved intermittently were fastest.
The range of nauplii velocities covered more than one order of magnitude
(O.mediterranea versus T.stylifera) and that of early copepodid stages about a
factor of two (P.quasimodo versus P.aculeatus). The range within a single taxon
could be large (E.hyalinus N, maximum was >400% of the minimum value) to
small (e.g. C.velificatus N, maximum was only 10% larger than the minimum). A
statistical comparison (same as for per cent activity) reveals no significant differences between adjacently positioned stages; however, stages once removed from
each other or more were usually significantly different (e.g. O.mediterranea N *
P.quasimodo N). We then calculated the distance traveled per minute by multiplying velocity by percent activity (Table V): lowest and highest values were more
than one order of magnitude apart. Nauplii and copepodids of P.quasimodo traveled farthest, and the intermittently moving nauplii of O.mediterranea and C.velificatus the shortest distances.
Description of motion paths
The motions of nauplii and copepodids, recorded in two dimensions, will be
described in three dimensions because of qualitative observations. Paracalanus
nauplii, either those of P.aculeatus (Figure 1) or P.quasimodo (Figure 2), moved in
spirals and therefore in three dimensions. The lines shown connect the front part
of their body, and the sticks protruding from the lines indicate the position of their
body (Figure 1). This means that the longitudinal axis of these nauplii is often
perpendicular to the direction of motion. The copepodid stages of these and other
Table IV. Velocity (mm s~') at which late nauplii and early copepodid stages of several copepod
species were moving
X
n
SE
Range
O.m.
N
5.24
7
±0.44
3.96.9
Cv.
N
2.73
8
±0.12
2.73.0
Rq.
N
134
4
±0.16
0.931.69
Cv.
C
Eh.
N
0.92 0.86 0.78 0.68 0.67 0.61
4
7
8
6
7
12
±0.15 ±0.08 ±0.09 ±0.07 ±0.09 ±0.07
0.56- 0.63- 0.53- 0.45- 0.44- 0.261.26 1.12 1.06 0.87 1.01 123
Rq.
C
Ep.
N
Ts.
C
Ra.
N
Ep.
C
0.61
5
±0.11
0.371.01
Ra.
C
0.48
5
±0.02
0.440.54
T.s.
N
0.39
4
0.014
0350.41
i, mean; n, number of animals; SE, standard error, N, nauplii; C, copepodid stages. Species abbreviations are self-explanatory from Table I.
Table V. Distance travelled per minute by each taxon (mm min'1
Rq. > Rq. > Cv. > Ep. > Tj. > P.O. > Eh. > Ra. > T.s. > Ep. > Cv. > O.m
N
C
C
C
N
C
C
N
N
N
N
N
FC
FC
FC
FC
FC
FC
FC
41
80
40
37
14
6
52
47
54
23
19
26
FQ produce feeding current.
1703
G.-A.Piffenhofer et al
start
end
= 0.5mm
Fig. L Motion behavior of a nauplius stage IV (N IV) of P. aculeatus (0.16 mm body length, velocity
1.69 mm s~'); the nauplius is shown intermittently in its natural position. The line connects the front
part of the nauplius' body, the sticks represent its body.
start
Fig. 2. Extended motion path of a N V of P.quasimodo.
1704
Motion of nanplii and early copepodids
genera are shown usually in the shape of the capital letter T, the horizontal bar
representing the first antennae (Al) and the vertical bar the body. The copepodid
stages of P.aculeatus for extended periods move only in one dimension (Figure 3),
and eventually move in a second dimension. Those of P.quasimodo (Figure 4)
move for a while in two dimensions (moving and sinking), occasionally making a
turn (Figure 4), thus covering a third dimension, always (except when sinking) creating a feeding current. Nauplii of T.stylifera, which create a feeding current, also
move mostly with their body positioned perpendicular to the direction of motion,
and create loops (Figure 5), resulting in three-dimensional coverage of the respective water mass. The large dot represents the front part of the body, followed by
the body and the two posterior setae of identical length which are characteristic
of T.stylifera nauplu. Late nauplii of T.turbinata display a motion behavior similar
to that of T.stylifera (Figure 6). Earlier and later copepodid stages of Temora
usually move in semicircular paths while feeding in configurations which hardly
differ from those of their late nauplii (Figure 7). Here, we show a copepodid stage
I—i = 0.5 mm
Fig. 3. Motion behavior of a copepodid stage V (C V) of P.aculeatus (0.83 mm body length, velocity
033 mm s~'>; (this copepodid's position is shown every 0.13 s); the cephalothorax is positioned vertically and the first antennae are sloping slightly.
Fig. 4. Motion behavior of a copepodid stage HI (C III) of P.quasimodo (0.42 mm body length, velocity 1.04 mm s"1); (the copepod'i position is shown intermittently every 0.13 s.The copepodid is shown
as the capital letter T, the vertical bar representing its body, the horizontal the Al.
1705
G.-A.PafTenbofer el aL
start
n=0.5mm
Fig. 5. Body position and motion path of a nauplius stage V (N V) of Tjtylifcrcr, the dot represents the
anterior part of its body, and the two diverging lines the two setae of even length at the animal's rear
(the body length of this nauplius is 0.24 mm).
I (C I) of T.turbinata over a period of 28 s as it moves slowly away from the
observer, at 0 s, we see the copepod from the rear, during the following 5 s, it moves
to the left, then turns to the right, is seen laterally at 7 and 8 s, and is observed again
from the rear at 9 s with its Al clearly visible. This animal is swimming ventral
upwards all the time, unless it relocates rapidly in the vertical (not shown here).
Late nauplii of E.hyalinus which do not appear to create a feeding current, mostly
move through the water more or less perpendicular to the longitudinal body axis
(Figure 9), as do in general late nauplii of E.pileatus (Figure 8). They, too, move
three-dimensionally.
Discussion
Historical perspective on motion of juvenile copepods
Planktonic copepods exist in two major morphological forms: the nauplius and the
copepodid stages (Storch, 1928). Storch described the development from nauplius
to copepodid as one of the major functional changes of the naupliar appendages.
The performances of planktonic copepods have repeatedly been related to their
morphology, particularly to that of the cephalic appendages of older copepodid
stages, adult females and males (e.g. Anraku and Omori, 1963; Gauld, 1966). The
1706
Motion of naoptii and early copepodids
\
\
\
start
I \\o
I
1 = 0.5mm
Fig. 6. Motion path and body position of a nauplius stage V (N V) of T.turbinata (023 mm body length,
velocity 0.50 mm s~').The dot represents the anterior part of the nauplius.
23
25
22
O
\_>
14
O
M
19
O
„
12
10sec
^
-Or
= o.5mm
Fig. 7. Motion path and body position of a copepodid stage I (C I) of T.turbinata (028 mm cephalothorax length, velocity 0.65 mm s~') over a period of 28 s; shown are body contours including the first
antennae; in the turns, this copepod moves away from the observer; between turns, it remains in the
same plane of view. The Al are visible as the copepodid turns, sticking out from its body.
1707
G.-A-P«ffenh6feT el aL
start
= o.5mm
Fig. 8. Motion path and body position of a nauplius stage V (N V) of E.pileatus (0.60 mm body length,
velocity 0.79 mm s~').The dot represents the anterior of the nauplius.
start
\
.fes
= o.5mm
Fig. 9. Motion path and body position of a nauplius stage (N V) of E-hyalinus (0.82 mm) body length,
velocity 0.63 mm s-').The dot is the front of the nauplius.
1708
Motion of naopBi and early copepodkb
performances of early juveniles received less attention, but were addressed in
several cases in considerable detail: the feeding behavior of nauplii (N IV-N VI)
of Diaptomus gracilis (Calanoida) and Cyclops strenuus (Cyclopoida) was studied
by Storch (1928). He concluded that the first antennae (Al) were used only for
occasional rapid locomotion.The second antennae (A2) and mandibles (Md) of
D.gracilis were thought to create a continuous feeding current directing food particles toward the mouth and also displacing the nauplius slowly, whereas those of
Cstrenuus worked similar to the Al, i.e. only occasionally once, or several times,
and therefore supported the locomotory function of the Al. Whereas the A2 and
Md of D.gracilis were thought to filter particles from the water current, those of
Cstrenuus were occasionally to grasp food particles. Storch briefly compared the
function of the appendages of the N VI of each of the two copepod species with
those of the C I.
The swimming and feeding of nauplius stage III (N III) and older ones of
Calanusfinmarchicus,Temora sp. and Acartia sp., and NIV of Oithona similis, was
investigated by Gauld (1958). He concluded that calanoid nauplii have two major
modes of swimming: smooth and slow gliding due to the motion of the A2 and Md,
and leaps due to strokes of all three pairs of mouth parts. Swimming of nauplii of
O.similis was always rapid and jerky, which was similar to that described by Storch
(1928) for Qstrenuus. Gauld (1958), however, found no evidence that nauplii of
calanoids and cyclopoids transported particles to the mouth by water currents.
When describing the developmental stages of various species of tropical and
subtropical planktonic copepods, Bj6rnberg (1972) emphasized nauplii even more
than copepodids. Her observations on the morphology and function of
appendages of nauplii and copepodids were summarized in two recent articles
(BjOrnberg, 1986a,b). The simplest locomotion of nauplii is that of Cyclopoida
including Oncaeidae: their three pairs of appendages move simultaneously backwards and forward like oars, resulting in uneven motion which is attributed to
their parallel musculature, as compared to those of calanoid nauplii which possess
intercrossing, and more powerful muscles resulting in smoother swimming.
Instar-specific swimming velocities were determined by Gerritsen (1978) for
nauplii, copepodids and adults of Cyclops scutifer, and by Landry and Fagerness
(1988) for three species of calanoids. Cinematographic observations revealed that
nauplii of E.pileatus and of Eucalanus crassus produced a feeding current by
motion of their A2 and Md.and used these mouthparts to direct individual phytoplankton cells towards their body, which were behaviors shown by their copepodid stages and adult females (Paffenhfifer and Lewis, 1989). Nauplii of E.hyalinus,
however, did not appear to create a feeding current and propelled themselves by
motions of their A2 and Md, and encountered food by actively swimming.
These previous observations revealed naupliar feeding currents of D.gracilis
(Storch, 1928), E.pileatus and E.crassus (BjOrnberg, 1972; Paffenhdfer and Lewis,
1989), but none for cyclopoid nauplii (Storch, 1928) and those of Cfinmarchicus,
Acartia sp. and Temora sp. (Gauld, 1958). Nauplii of cyclopoid copepods moved
with occasional leaps (Storch, 1928; Gauld, 1958; Gerritsen, 1978; Drits and
Semenova, 1984), as did copepodid stages of Oithona davisae (Uchima and
Hirano, 1988).
1709
G.-A J"illcnh6fer et aL
Our recent observations comparing motion between genera, closely related
species and stages were intended to improve our understanding of the similarities
and ranges of behavior of motion created by copepods. One shortcoming of our
study was the dissimilarity of food types, and that of experimental volumes. The
latter, however, were usually increased with increasing stage as we had assumed
increased motion with increasing stage. Food concentrations, although not excessively high, were thought to be above or near the satiation levels which are usually
much lower for nauplii and early copepodids than for adult females (Harris and
Paffenhdfer, 1976).
Ontogenetic changes
Among our general findings were that all calanoid copepodids produced a feeding
current, but not all the species' nauplii; and that nearly all the calanoid nauplii and
copepodid stages studied were near 100% active (except C I of E.pileatus), and
moved in three dimensions (except nauplii of Cvelificatus). How could we categorize these behaviors and compare them to planktonic cyclopoids? On the more
active side we placed the Temoridae (including observations on T.turbinata), the
late nauplii and early copepodids of which all created a feeding current and moved
100%; on the passive side were the late nauplii of O.mediterranca (and Oithona
plumifera, qualitative observations) and the adult females of O.plumifera which did
not create a feeding current and moved only 0.85% of their time (n = 3, personal
observation). Oithona spp. females in Antarctic waters remain, most of the time,
motionless (Atkinson, 1995). These observations on the activity of adult females of
Oithona differ from those of Uchima and Hirano (1988), who found much higher
activities for females of O.davisae in experiments conducted in 15 ml dishes.
Eucalanus pileatus nauplii were almost identical in behavior to those of Tstylifera,
but did not move their Al at all except when leaping (similar to copepodid stages);
however, the C I were only active 52% of the time. Nauplii and copepodid stages
of the Paracalanidae all moved nearly 100% of the time. Among the calanoid late
nauplii, those of Cvelificatus stood out because they moved occasionally, which
was similar to that of cyclopoid nauplii (Storch, 1928; Gerritsen, 1978; Drits and
Semenova, 1984). Their C I and CII, however, displayed a motion behavior which
was close to that of other studied calanoid species (Table III).
Landry and Fagerness (1988) quantified the horizontal and vertical swimming
velocity of nauplii and CI of Calanus pacificus,Acartia clausii and Pseudocalanus
sp. NIV or V of each species swam faster than the respective C I. This is similar to
our observations on Paracalanidae and E.pileatus (Table V), and contrary to
Cvelificatus and T.stylifera. However, Cvelificatus nauplii swim faster than their
early copepodids if the break periods are excluded (Table IV).
Pronounced ontogenetic changes of motion and behavior were observed for
Cyclops scutifer (Gerritsen, 1978). Their swimming speeds increased from nauplius to adult females Nauplii were mostly motionless, relocating with occasional
leaps, while C Is leapt occasionally and spent most of the time sinking, and late
copepodids and adults displayed a frequent hop and sink pattern, i.e. active movement increased from nauplius to adult female. For Acartia tonsa, swimming speeds
1710
Motion of naoptij and early copepodfata
increased from early nauplius to about N VI or C I, then remained rather even at
0.7-0.8 mm s"1 until C TV, and reached 1.4 mm s"1 for adults (Buskey, 1994).
In essence, a range of ontogenetic behavioral changes was observed for
calanoids. There was little difference between naupliar and post-naupliar stages of
T.stylifera except for velocity; some differences among the Paracalanidae as
nauplii did not create a feeding current and swam faster, and major differences for
Cvelificatus: its nauplii moved occasionally, early copepodids continuously, and
adult females alternated between swimming and sinking. Oithona plumifera
(qualitative observations for nauplii) was similar to T.stylifera, i.e. hardly any
ontogenetic behavioral differences were observed.
Motion in space
Depictions and descriptions of the motion of juvenile copepods, despite their
ubiquitous occurrence, are rare: Bjornberg (1972) displayed locomotion of nauplii
of Clausocalanus furcatus and Acartia sp.; Gerritsen (1978) described the motion
of nauplii and various copepodid stages of Cyclops scutifer, Bjdrnberg (1986a)
presented drawings from Bresciani (1960) on the motion of nauplii of Oithona,
Acartia, Paracalanus and a harpacticoid;Uchima and Hirano (1988) illustrated the
motion of copepodid stages of Oithona davisae. Shuvayev (1978), who observed
nauplii of five copepod species, found 'no differences in the movement of nauplii
of these species'.
Our observations indicate that nauplii of the genera Eucalanus, Paracalanus
and Temora, which all move near 100% of the time, are moving in three dimensions over periods of several seconds and distances of several millimeters (Figures
1,2,5,6,8 and 9), i.e. small-scale patchiness of food particles can be explored. The
patterns of calanoid naupliar motion differ among genera. Whereas Paracalanidae
move in successive small loops, similar to Cfurcatus (BjOrnberg, 1972) and Acartia
sp. (Bjdrnberg, 1986a), the Temoridae and Eucalanidae move in larger, more
irregular circles, and sometimes even straight. On occasion, Temora nauplii move
in narrow helical motions in one direction when relocating vertically (not shown).
The velocity and motion of nauplii which create a feeding current can vary, as
observed for E.pileatus: it is hypothesized that the nauplius changes the angles of
position of its A2 and Md, thus creating a more pronounced feeding current when
moving slowly and less when moving fast.
Concerning copepodid stages, we observed major differences within the genus
Paracalanus. Whereas those of P.quasimodo, a neritic species, operate in three
dimensions by moving and sinking (Figure 4), those of P.aculeatus, an outer
shelf/oceanic species, appear to move, over periods of -10-60 s, mainly in one
dimension (Figure 3). They do change directions suddenly by -90° at the abovementioned intervals. We assume that P.aculeatus, usually living in low food levels,
cannot afford to spend energy by turning its feeding current off and on at brief
intervals, as acceleration of the feeding current implies additional energy expenditure which the neritic P.quasimodo can afford at higher food levels. Early
copepodid stages of T.turbinata and T.stylifera move continuously in semicircular
motions with intermittent short straights (Figure 7).
1711
G.-A.Paffenb6fer et al
The significance of a feeding current has been addressed repeatedly (e.g. Strickler, 1982,1985; Paffenhttfer and Lewis, 1990), mostly in studies on late copepodid
stages and adult females. It allows the feeding copepod to explore an additional
dimension as water is displaced from a direction other than the one towards which
it swims. That dimension reaches from about half to more than one body length,
depending on the strength of the feeding current. The significance of a feeding
current should grow with increasing copepodid stage as food concentrations at
which a calanoid satiates increase by about a factor of 10 from N V to adult female
of Paracalanus sp. (Ambler, 1986). Different species seem to use different strategies of motion to encounter sufficient food: moving continuously in three dimensions and faster than their early copepodid stages (Figures 1 and 2,Table IV), which
change direction occasionally (Figures 3 and 4, and the text), should enhance the
chances of the 'non-feeding-current' nauplii of the Paracalanidae encountering sufficient food as compared to the post-naupliar stages. Late nauplii of T.stylifera,
which are only slightly larger than those of the Paracalanidae, move significantly
slower than their early copepodids and the Paracalanus nauplii (Table IV), but
compensate for the slower motion by creating a feeding current. How do the
amounts of water passing by a late nauplius of Paracalanus and Temora compare?
As P.quasimodo and P.aculeatus move forward, their second antennae with
extended setae plus body cover an area of 0.035 mm2; at 0.92 mm s"1 (Table IV),
the former covers 2.78 ml day-1, the latter 2.03 ml day 1 at 0.67 mm s"1. A T.stylifera N V draws water toward itself at 0.7 mm s"1 (SE = ± 0.065, n = 11) at a distance
of 02 mm from its body with a feeding current of 0.038 mm2. This results in 2.28 ml
of water being drawn per 24 h past this nauplius' body. These calculations reveal
that late nauplii of both genera appear to have similar volumes of water passing by
their body and appendages per day, although the modes of displacing water past
their appendages differ. These calculations are only approximations toward the
actual amount of water scanned by a nauplius as it tries to obtain food. The ingestion and clearance rates are a function of particle quality, size and concentration,
and the physiological condition of the copepod (Paffenhdfer and Lewis, 1990).
Significance of interspecies comparisons
This approach has been conducted previously mainly for swimming, often in conjunction with feeding, and then mostly with adult copepods (e.g. Lowndes, 1935;
Gauld, 1966; Shuvayev, 1978; Minkina, 1983; Greene, 1988; Landry and Eagerness,
1988; Tiselius and Jonsson, 1990). Landry and Eagerness (1988) and Tiselius and
Jonsson (1990) conducted a thorough evaluation between different species. Comparing seven species of facultative or obligate carnivorous copepods, maximum clearance
rates on preferred calanoid nauplii by six of the seven species were highly correlated
with mean predator swimming speed, and also with relative swimming speed, which
is the product of predator and prey swimming speeds (Landry and Eagerness, 1988).
The basis for this general finding is that the authors chose to emphasize analysis on
the prey species and stages preferred by therespectivepredators.
Tiselius and Jonsson (1990) compared the motion behavior, including mouthpart
activity, of adult females of six calanoid species. They categorized these species into
1712
Motion of nanpIB and early copepodids
three groups: (i) slow moving to stationary, (ii) fast swimming alternating with
sinking; (iii) sinking alternating with short jumps Among (i) was Temora longicornis which moved 99% of the time, which coincides with our findings on Temoridae,
and Paracalanus parvus moving 48% of the time. The latter implies intermittent
sinking similar to what we observed for C m of P.quasimodo (previously thought to
be P.parvus) which actively moved 78% of the time and sank intermittently (figure
4, and unpublished observations). Category (ii) was represented by two Centropages
species which actively moved 27-58% of the time (upward) and sank intermittently,
which was similar to the behavior oiCvelificatus females (MH.Bundy,unpublished
observations). Category (iii) was represented by Acartia chusiiv/hich spent 87-99%
of its time sinking with frequent intermittent jumps. Assessing our observations in
conjunction with those ofTiselius and Jonsson (1990), we may present the following
general categories, (i) Continuous activity: examples are the T.stylifera and
T.turbinata (nauplii, copepodids, adult $). However,Van Duren and Videler (1995)
observed that late nauplii of Temora longicomis spent 57% (no food offered) to 69%
of the time (high food concentration) swimming, whereas C I moved nearly 100%
of the time independent of food concentration, (ii) Changes in activity: with increasing copepodid stage P.quasimodo spends more time sinking; drastic modifications
seem to occur with the Centropagidae, the nauplii of which move only occasionally,
whereas the early copepodids move continuously followed by adult females which
alternate frequently between swimming and sinking, (iii) Occasional activity:
Oithonidae (nauplii, copepodids, adult $), which is supported by findings of Drits
and Semenova (1984). This categorization should be interpreted with caution
because variations in food concentrations and predation pressure could alter motion
behavior. The percentage of time spent feeding by adult females of A.tonsa
decreased from 98.4% at 03 mm31"1 to 81.7% at 3.0 mm31"1 of phytoplankton (Saiz,
1994). The presence of the predaceous copepod Epischura nevadensis reduced the
clearance rate of Diaptomus tyrrelli by as much as 60% (Fblt and Goldman, 1981).
What do these behaviors imply for predation? In a model on predator-prey
interaction, Gerritsen and Strickler (1977), using encounter probabilities, found
two optimal strategies for predators: (i) cruising predators would prey most successfully on slowly moving prey and (ii) ambush predators on prey which moved
fast. They concluded that the best strategy for prey to minimise encounters with
predators would be to move slowly.
We observed a range of motion behaviors from intermittently but fast moving
nauplii (e.g. O.mediterranea), to relatively fast but continuously moving animals
(e.g. nauplii and copepodids of P.quasimodo), to continuously and slowly moving
nauplii {T.stylifera). A continuously and slowly moving animal provides a weak
and continuous signal, a fast but brief moving one a temporary but strong signal.
We believe that a combination of velocity (signal strength) and its duration (signal
longevity) will determine the probability of encounter.
However, encounter of prey and predator is only part of a potential predation
process. Similar motion of similarly sized animals (e.g. P.quasimodo late nauplii
and early copepodids) will result in similar encounter frequency, but in dissimilar
predation as the late nauplii are eaten in a far higher percentage than the early
copepodids (Landry, 1978). Perceptive ability and the strength of the reaction to
1713
G.-AJ"affenh6fer et al
such perception should determine the outcome of a predator-prey encounter (e.g.
Paffenhdfer, 1991). We will address this subject in a forthcoming paper.
The comparison of six (Tiselius and Jonsson, 1990) and seven (Landry and Fagerness, 1988) species of adult females of planktonic copepods has shown us the wide
range of behavior characteristics among species and, to some extent, within single
species To this we add the ontogeny of behavior which could be used for taxonomic
and phylogeneric considerations (Tinbergen, 1963). Bj6rnberg (1986b) uses the
motion behavior of nauplii to differentiate among species of the genus Eucalanus
and to develop phylogenetic considerations. Evaluations of naupliar musculature
were also used for taxonomic purposes (BjOmberg, 1986a, p. 59). Huys and Boxshall
(1991), in their new phylogeny of the Copepoda, relied largely on morphological
and anatomical features of adults, in conjunction with some ecological observations.
In a panel discussion on Copepod Phylogeny (1986), BjOrnberg emphasized the significance of observations on juveniles, particularly nauplii, to phylogeny.
Our findings, in conjunction with previously published data, illustrate that
observations on juvenile behavior should enhance our understanding of the performance of copepods in a continuously dangerous environment, i.e. the ocean.
Acknowledgements
This research was supported by two grants from the National Science Foundation
(OCE 90-00144 and 93-19226). The constructive comments of two anonymous
reviewers contributed to improve this manuscript
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Received on July 31,1995; accepted on April 11,1996
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