Centropages behaviour: Swimming and vertical migration

Progress in Oceanography Progress in Oceanography 72 (2007) 121–136 www.elsevier.com/locate/pocean

Centropages behaviour: Swimming and vertical migration Miguel Alcaraz *, Enric Saiz, Albert Calbet Institut de Cie`ncies del Mar, CSIC. P. Marı´tim de la Barceloneta 37-49, 08003 Barcelona, Spain Available online 13 January 2007

Abstract The evolutionary success of any species living in a variable environment depends on its capacity to enhance the probability of finding food and mates, and escaping predators. In the case of copepods of the genus Centropages, as in all planktonic copepods, their swimming behaviour is closely tied to these vital aspects, and shows a high degree of plasticity and adaptive capacity. Swimming mechanisms of Centropages change radically during development, mainly in the transition between naupliar stages to the 1st copepodite; nauplii do not produce feeding currents, whereas copepodites do. Adults and late developmental stages of C. typicus, C. hamatus and C. velificatus spend most of the time in slow swimming and resting breaks, with occasional and brief fast swimming (escape reactions) and grooming events. Slow swimming is closely related to the creation of feeding currents, and results from the beating of the cephalic appendages in a ‘‘fling and clap’’ manner. The proportion of time allocated to the different swimming activities depends on sensory cues like type and concentration of food, presence of potential mates, light intensity, hydrodynamic flow, etc. The responses of Centropages to changes in flow velocity fluctuations (small-scale turbulence) are similar to the escape responses (fast swimming) triggered by the presence of potential predators. Centropages generally have standard nocturnal vertical migration patterns involving considerable vertical displacements. This behaviour is closely related to the narrow spectral sensitivity and the low intensity threshold of the genus, and has important consequences for the active vertical transport of matter and energy. The variety of responses of Centropages to environmental changes, and in general all the aspects related to its swimming behaviour seem to be controlled by the trade-off between energetic gains (food intake), losses (swimming energy expenditure), and predation risk. Behavioural plasticity and adaptation appear to be the most relevant characteristics for the success of the genus in a wide range of marine environments.  2007 Elsevier Ltd. All rights reserved. Keywords: Copepods; Centropages; Swimming behaviour; Vertical migration

1. Introduction Living suspended in a three dimensional aquatic world is a common feature of all planktonic organisms, their behaviour being a direct consequence of the physical, chemical and biological properties of their surrounding environment. Amongst zooplankton, copepods live at the border between the viscous and the inertial worlds (Naganuma, 1996). This is due, in part, to their body-size (and that of the appendages involved in *

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the different activity mechanisms), and in part to the range of velocities of their motion (Strickler, 1975b; Yen, 2000). In most Calanoids swimming includes several motion activities that alternate, from smooth slow swimming, that requires the rapid motion of the small cephalic appendages and is tightly related to the creation of feeding currents, to fast-swimming or escape reactions (Alcaraz et al., 1980; Strickler, 1982; Paffenho¨fer et al., 1982). By direct observation it is possible to obtain some insights into the copepods’ motion behaviour, such as their individual patterns of vertical migration or the creation of swimming currents (Gauld, 1958). However, the study of the details of their behavioural repertoire requires techniques that allow observation at appropriate space and time scales (Alcaraz et al., 1980; Paffenho¨fer et al., 1982; Strickler, 1975b). The same applies to the different components of copepod motion (Strickler, 1977), as well as to their quantitative analysis (Cowles and Strickler, 1983; Paffenho¨fer et al., 1982; Strickler, 1984), and modelling (Caparroy and Carlotti, 1996; Caparroy et al., 1998). Understanding the characteristics of the temporal motion patterns (Tiselius and Jonsson, 1990), and the changes induced by environmental conditions (Costello et al., 1990; Marrase´ et al., 1990; Paffenho¨fer et al., 1996; Titelman and Kiørboe, 2003a,b), allows the perception that copepods have of their world to be better understood. The richness of copepods’ behavioural responses is closely related to the existence of a sensory system including, in addition to rudimentary photosensors, a complex array of mechano- and chemoreceptors (Barrientos, 1980; Strickler, 1975a). In most Calanoids, displacement by slow swimming requires the rapid motion of small appendages and is directly involved in the process of food acquisition by the creation of feeding currents (Alcaraz et al., 1980; Paffenho¨fer et al., 1982; Strickler, 1982). Slow swimming has a more direct influence on the detection, capture and handling of food, simultaneously allowing the animal’s displacement by slow gliding. These motion patterns result in low Reynolds numbers and laminar water flow regimes that have, from the point of view of the energy expenditure, a low cost (Alcaraz and Strickler, 1988; Vlymen, 1970). Other displacement mechanisms involve in adult copepods all the limbs, from antennae to thoracic legs. These mechanisms result in high-speed motions, escape reactions that reach speeds of 500 body lengths per second, and accelerations as high as 1200 cm s 2. The consequences are high Reynolds numbers and turbulent flow regimes (Strickler, 1975b). From the point of view of energy consumption such behaviour can be around 400 times more expensive per unit time than the normal, cruising displacement by slow swimming, or the ‘‘hop and sink’’ motion typical of Cyclopoids (Alcaraz and Strickler, 1988; Marrase´ et al., 1990; Strickler, 1975b). Water viscosity and the organism negative buoyancy determine the other two components of the swimming behaviour of Calanoid copepods: grooming and resting breaks. By grooming, the organism gets rid of food and detritic particles accumulated by the viscous properties of water in or near the feeding, swimming and sensory limbs, reducing their efficiency. During resting breaks, they stop the appendage motion and slowly settle due to their negative buoyancy (Strickler, 1982), allowing the exploration of the environment in the search for physical or chemical signals of food, mates and predators, in an undisturbed, descending mode. Finally, diurnal migration, a direct consequence of oriented swimming mechanisms, is probably one of the most intriguing ecological aspects of copepod behaviour. Partly externally induced and partly endogenous, this may result in active vertical transfer of matter, and has important consequences for the functioning of pelagic systems, especially for oligotrophic ones (Alcaraz, 1988; Saiz and Alcaraz, 1990). Here we will describe and discuss the aspects related to the motion behaviour of Centropages typicus, complemented with data for two other species: C. hamatus and C. velificatus. Together with C. typicus these species comprise most of the literature on the genus, and can provide a comprehensive insight of the ecological relevance, specificity and ontogenic peculiarities of their motion behaviour. 2. Swimming of adults and late copepodites By direct observation of copepods only gross details or macroscopic aspects of their swimming behaviour can be identified. In this way we can easily identify periods of smooth swimming, interspersed with motionless breaks, eventual fast and brief escape reactions, and ‘‘grooming’’. Similarly, the pumping of water by the motion of appendages in a way similar to that of the wings of a butterfly is quite evident (Cannon, 1928). However, the small size and high velocity of the appendages involved require the use of high spatial and tem-

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poral resolution methods to decompose the motion pattern. This improvement in resolution can be obtained by high-speed micro-cinematography (Alcaraz et al., 1980; Paffenho¨fer et al., 1982; Strickler, 1977; Strickler, 1982), and micro-impedance techniques (Gill, 1987; Poulet and Gill, 1988). In both cases it is necessary to tether the organisms, either to keep them in focal plane of the optical system, or to obtain clear micro-impedance records of the moving parts. In Calanoids, the smooth gliding and the slow swimming result from a very precise succession of movements of the cephalic appendages (exo- and endopodites of maxilipeds, 2nd antennae and maxillae, Fig. 1) defined as a ‘‘fling and clap’’ motion (Strickler, 1984). Apart from the propelling effect, this behaviour is rigidly linked to the feeding activity of the organism by the creation of feeding currents. These entrain food particles as well as chemical information (Strickler, 1982, 1984), and in turn help to create specific hydrodynamic and chemical trails, essential signals for triggering many aspects of copepod behaviour. By means of high-speed cinematography (500 frames per second), Cowles and Strickler (1983) estimated the motion frequency of the cephalic appendages of Centropages typicus to be of the order of 50 Hz. The individuals were tethered in a suspension of 4 ppm by volume of Gymnodinium nelsoni. These authors described many details of the movements of C. typicus, such as, for instance, the figure of eight-shaped pattern drawn by the tips of the second antenna and maxiliped, whose motion is 180 out of phase. In another study, Poulet and Gill (1988) obtained lower frequencies (36.5 Hz, Fig. 1), by the spectral analysis of the recorded motion of copepod limbs using a computer micro-impedance system. Apart from the study of the motion pattern of cephalic appendages, Cowles and Strickler (1983) also described the different activities that make up the swimming behaviour of C. typicus (slow swimming, resting breaks, escape reactions, and grooming, Table 1), and analysed the changes observed in the time-pattern (frequency and duration) of slow swimming and breaks in relation to the food environment. An essential question to interpret these results is whether tethering modifies the behaviour of copepods. According to Hwang et al. (1993), restrainment has no effects on the time allocated to the different behavioural activities, although the

ANGLE (deg.)

a

40 24 8 -8 -24 0.1

0.2

0.3

0.4

0.5

TIME (seconds)

AMPLITUDE mV

b 100 E

S 0

1 sec. Fig. 1. (a) Time pattern of the movement of the endopodite of the 2nd antenna of a Calanoid copepod (Eucalanus crassus) filmed at 500 fps. (b) Beat pattern of 1st maxilla of Centropages typicus (micro-impedance techniques). Modified from Strickler (1984) and Poulet and Gill (1988).

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Table 1 The four activity modes that make up the swimming behaviour of adult C. typicus, and are also common in other Calanoids Activity

Description

Occurrence

Slow swimming

Directly related to the creation of feeding currents, consists in the rhythmic motion of cephalic appendages (second antennae, first maxillae and maxilipeds) Organism at rest, without moving the appendages Rhythmic swimming thrusts with the thoracic legs, sometimes with flipping antennae and a thrust or beating of the abdomen Cleaning of the antennulae by brushing them through part of the cephalic appendages (mouthparts). Maxillae and 2nd antennae brushed by maxilipedes

Frequent

Breaks Fast swimming and escape reactions Grooming

Frequent Rare Occasional

Modified from Cowles and Strickler (1983).

resulting flow fields could to be partially affected (Alcaraz et al., 1980), therefore validating the results of Cowles and Strickler (1983). The frequency and duration of slow swimming bouts and rests in Centropages (Table 2) depend of the characteristics of the food offered during experimentation (i.e., mixed assemblage, non-motile like diatoms, motile like dinoflagellates or ciliates, mixed natural food, etc.), and of its abundance (Fig. 2). The time allocated by the different species of Centropages to slow swimming (creation of feeding currents), as well as the frequency and amplitude at which cephalic appendages are beaten are directly related to the concentration of food, and inversely to the time at rest (Caparroy et al., 1998; Cowles and Strickler, 1983; Hwang et al., 1993; Tiselius and Jonsson, 1990). At high food concentrations, the velocity of C. velificatus is similar to that of C. hamatus (Tiselius and Jonsson, 1990), the velocity being inversely related to the duration of swimming bouts. Simultaneously, the shape of the swimming path is more twisted (Fig. 3), resulting in ratios between net and gross displacement rate (NGDR) about half of those observed at low food conditions. The motion in high-food conditions is based on alternate bouts of swimming-sink, on occasions looping, with vertical upward movements after sinking, in order to search more efficiently a given water volume. At low-food conditions, the motion consists in leaping after sinking in order to move from one water volume to another, in a way similar to the behaviour described by Cowles and Strickler (1983). This behaviour indicates that the organism perceives the trophic environment (i.e., food concentration, intensity of chemical food trails, etc., Jackson and Kiørboe, 2004; Poulet and Gill, 1988), and adjusts the motion of the appendages, the frequency of slow swimming events, and their duration accordingly. At low food concentration, the copepod propels itself in search of the stimulus (food) while maintaining the balance between the metabolic losses due to displacement (although low), and the energy acquired with food. During the resting phase, the organism descends, sinking out from zones where food is absent while exploring the water for chemical or hydrodynamic cues until locating either an area with higher food concentration, or the track of a mate or a predator. The other two motion activities that make up the swimming behaviour of Centropages (fast swimming, or escape reactions, and grooming) occupy proportionally smaller fractions of the temporal motion pattern under undisturbed hydrodynamic conditions. Fast swimming (escape reactions) is a highly energy consuming activity, and consists in strong, rhythmic leaps with the thoracic legs, with occasional flinging of antennae and abdomen. A similar, albeit much less energy-consuming activity, is the leaping with the legs, antennae and abdomen in the hop and sink swimming mode of some Cyclopoids (Alcaraz and Strickler, 1988). The fast swimming events (escape reactions) can interrupt either a slow swimming or a break period (Costello et al., 1990). Their frequency (0–14 events min 1, C. hamatus, Tiselius and Jonsson, 1990) and duration (0.1– 1.5 s, Cowles and Strickler, 1983) depends upon the intensity of the stimulation, either hydrodynamic (Marrase´ et al., 1990; Strickler, 1977), or chemical, as observed in other copepod species (Poulet and Gill, 1988). The fraction of time allocated to fast swimming by Centropages in calm (undisturbed) conditions (Table 2) is also a function of the food concentration, although the response is nonlinear (Costello et al., 1990). Although in undisturbed conditions the contribution of escape reactions to the bulk of energy consumption is not very important, certain chemical (i.e., pheromones), hydrodynamic (small-scale turbulence), or luminous stimuli enhance the frequency of escape reactions in copepods, thus determining a significant rise in the energy allocated to swimming (Marrase´ et al., 1990). Finally, grooming events, although not strictly

Table 2 Fraction of time allocated to slow swimming, breaks, and fast swimming + grooming by adult Centropages typicus and Centropages hamatus under different food conditions and in still water Species

Light conditions

Food concentration

Recording modality

Slow swimming

Breaks

Fast swimming + grooming

Author

C. typicus

Day

a

Prorocentrum micans

3.5–4 ppm(volume)

Tethered

2.11(80.4)

0.38(10.6)

0.1–1.5(9.4)

1

Day

a

Gymnodinium nelsoni

3.5–4 ppm(volume)

Tethered

1.38(51.2)

1.30(43.3)

0.1–1.5(5.5)

1

C. typicus

Day

a

Prorocentrum micans

0.35–0.4 ppm (volume)

Tethered

0.8(46.6)

0.87(49.6)

0.1–1.5(3.8)

1

C. typicus

Day

a

Gymnodinium nelsoni

0.35–0.4 ppm (volume)

Tethered

2.59(60.5)

1.75(39.5)

–

1

C. typicus

Day

a

Filtered sea water

–

Tethered

0.98(19.2)

4.08(80.5)

0.1–1.5(0.3)

1

C. typicus

Natural food

b

Free swimming

1.9(42)

–(56)

–(2)

2

1.7 lE m

2 1

Natural food

b

Free swimming

4.0(42)

–(56)

–(2)

2

1.7 lE m

2 1

Filtered sea water

–

Free swimming

–(49.5)

–(50.4)

–

4

C. typicus

1.7 lE m

2 1

s

Strombidium sulcatum

1 cell/ml

Free swimming

–(79.5)

–(20.5)

–

4

C. hamatus

220 lE m

2 1

Natural food

b

Free swimming

0.4(27)

–(70)

–(3)

2

C. typicus C. typicus C. typicus

220 lE m

2 1

s

s s

s

2 1

C. hamatus

1.7 lE m

Natural food

b

Free swimming

0.6(41)

–(59)

–

2

C. hamatus

Daya

Filtered sea water

–

Tethered

0.50(20.6)

2.82(78.9)

2.99(0.5)

3

C. hamatus

Daya

Filtered sea water

–

Free swimming

0.51(27.2)

1.37(72.4)

1.48(0.4)

3

s

Average duration in seconds of each behavioural activity, and % time allocated (in parentheses). Modified from: 1 = Cowles and Strickler (1983). 2 = Tiselius and Jonsson (1990). 3 = Hwang et al. (1993). 4 = Caparroy et al. (1998). a Unknown light intensity. b Unknown food concentration.

M. Alcaraz et al. / Progress in Oceanography 72 (2007) 121–136

Food type

125

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M. Alcaraz et al. / Progress in Oceanography 72 (2007) 121–136

a

FILTERED SEAWATER

40 20

SLOW SWIMMING

0 40 20

BREAKS 0

b

P. MICANS: 400ml-1 40

FREQUENCY

20

c

SLOW SWIMMING

0 40 20

BREAKS

0 P. MICANS: 40ml-1

40 20

SLOW SWIMMING

0 40 20 0

BREAKS 0

1

2

3

4

5

6

7

8

9

10

DURATION OF ACTIVITY(s) Fig. 2. Frequency of duration bouts of slow swimming (S.S.) and breaks (Br) in (a) filtered seawater, (b) low food concentration (P. micans, 40/ml), and (c) high food concentration (P. micans, 400/ml). Modified from Cowles and Strickler (1983).

related to swimming behaviour, are directly related to food concentration, their duration ranging from 0.1 to 1.5 s (Cowles and Strickler, 1983). A consequence of copepod swimming is the formation of a variety of flow structures, hydrodynamic disturbance and vortices. These result from the combination of the flow created by the motion of appendages and the organism displacement (Fig. 4). These structures usually either delimitate or disperse chemical trails of prey, predators or potential mates (Bundy and Paffenho¨fer, 1996; Fields and Yen, 1997; Van Duren and Videler, 1995; Van Duren et al., 1998). 3. Motion in early developmental stages Although nauplii and early copepodites represent the most abundant metazoans globally, the details of their motion, responsible for their success against predation, are less well known than for older developmental stages (Gauld, 1958; Paffenho¨fer and Lewis, 1989). It is in the transition between the last naupliar stage to the first copepodite that the major morphological changes take place, and where the swimming activity shows key behavioural differences (Landry, 1978; Paffenho¨fer and Knowles, 1980; Paffenho¨fer et al., 1996). While most copepodites of the Calanoid copepods studied to date create feeding currents when moving by slow swimming, not all the nauplii of different copepod species do (Paffenho¨fer et al., 1996). Cyclopoid nauplii exhibit a simple behaviour due to their muscular simplicity, whereas Calanoids, with complex, intercrossing musculature, can perform elaborate movements (Bjo¨rnberg, 1972). Amongst Calanoids, there are broad spe-

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127

Paths in High Food draw to scale

Hi2 53.2sec

Hi3 42.1sec

Z Hi1 47.5sec

20mm

X Y Paths in Low Food draw to scale

Lo1 26.7sec

Z

Lo3 18.7sec

Lo2 20.3sec

20mm

X Y Fig. 3. Effects of food concentration on the velocity and shape (convolutions) of swimming paths of Centropages velificatus. (a) High food concentration. (b) Low food concentration. After Bundy et al. (1993).

Fig. 4. Hydrodynamic disturbances created by a planktonic crustacean while swimming (Daphnia sp. Schlieren optics Author: J.R. Strickler).

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cies-specific and stage-specific differences in locomotion. From the point of view of swimming mechanisms, the only characteristics shared by nauplii and copepodites are that both, with few exceptions, are active most of the time, and move in a three dimensional pattern (Paffenho¨fer et al., 1996). The differences in body structure account for most of the differences in motion mechanisms of nauplii and copepodites, as well as for the different ways in which common problems of behavioural activity have been resolved. According to Titelman and Kiørboe (2003a), the motion of nauplii of most copepod species can be classified into two groups. Some nauplii swim in a hop (jump) – sink motion, moving intermittently, doing simple leaps and being active a very small percentage of time (Type A), while others swim continuously (Type B). The nauplii of the genus Centropages exhibit both swimming modes, C. typicus being a type B swimmer, whereas C. velificatus is a type A. The characteristics of the swimming behaviour of both species (temporal pattern, velocity, frequency of events, Table 3) are very different, as are their ontogenic changes. C. velificatus nauplii move intermittently once every 5–20 s, significantly faster than copepodites, although most of the time they are motionless. Therefore, the distance travelled is very small. Another noticeable difference is that C. velificatus nauplii do not produce feeding currents, whereas copepodites do. In the case of C. typicus, nauplii swim almost continuously in a helicoidal pattern (Titelman and Kiørboe, 2003a) likely the result of slow smooth gliding produced by the continuous motion of the first and second antennae and mandibles, with a few brief breaks. Early nauplii (NI-II) swim more continuously than NIV-V, but in older nauplii the path is more regular, following a helicoidal pattern (Fig. 5). We must take into account, however, that the swimming patterns

Table 3 Motility characteristics of early developmental stages of Centropages typicus and C. velificatus under different food conditions C. typicus(1)

Frequency of motion Feeding currents Food Swimming Sinking Jumping Swimming velocity Sinking velocity Jumping velocity

C. velificatus(2)

NI-II

NIV-V

NII-IV

CI-II

Frequent

Frequent

Occasional

Frequent

Unknown Filtered sea water 94.8(10.1) 5.12(10.1) 0.1(0.1) 0.33(0.21) 0.05(0.04) 4.10(1.27)

Unknown Filtered sea water 98.0(2.0) 1.7(2.0) 0.2(0.2) 0.72(0.31) 0.14(0.07) 10.40(1.84)

No Rhodomonas baltica + Gymnodinium nelsoni 8.5(1.5) – – 2.73(0.12) – –

Yes Rhodomonas baltica + Gymnodinium nelsoni 100(0) – – 0.86(0.08) – –

Frequency of events, creation of feeding currents, and velocity for the different activities in mm.sec 1. In parentheses: SD. Modified from: (1) Titelman and Kiørboe (2003a,b); (2) Paffenho¨fer et al. (1996).

b

late Centropages

6

6

4 8

2

Y (m

m)

0

0

m (m

4

2

)

4 6

X

0

8

2

6

0

6 4 6

2 4

2

0

0

(m

2

4

)

Z (mm)

8

Z (mm)

8

m

early Centropages

X

a

Fig. 5. Swimming tracks (3D) of early and late nauplii of Centropages typicus in 0.2 lm filtered seawater. (a) Early nauplii (N I-II, trail 125.2 s). (b) Late nauplii (N IV-V, trail 90.1 s). Modified from Titelman and Kiørboe (2003a,b).

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and velocities described for both species of nauplii correspond to undisturbed, hydrodynamically stable situations. When Centropages nauplii detect hydrodynamic disturbances similar to those generated by predators, the response consists of escape jumps for defined fluid-deformation rates, the escape distance increasing with age (Titelman and Kiørboe, 2003b). 4. Water motion and swimming pattern The effects of water motion on plankton depend on the space and time scales of the flow, and on the size of the organisms. While at large- to macroscale the flow cannot be sensed by zooplankters, small- to microscale fluid motions (i.e., small scale turbulence) can affect individual behaviour for copepods as small as 1 mm (Yamazaki and Squires, 1996; Alcaraz, 1997). The small-scale changes in the velocity field have two main effects. First, the changes in the velocity components of suspended particles increase their encounter probability (Rothschild and Osborn, 1988). As a consequence, the food concentration as perceived by copepods is enhanced (Marrase´ et al., 1990), and the number and duration of feeding (slow swimming) bouts increases (Costello et al., 1990; Hwang et al. (1994)). The second effect depends on the capacity to detect small-scale turbulence. This is accomplished by mechanoreceptors, modified cilliary structures distributed along antennae and other parts of the body of copepods (Strickler, 1975a; Barrientos, 1980; Bundy and Paffenho¨fer, 1993). These structures are able to detect flow oscillations ranging from 40 to 1000 Hz, and setal displacements of 10 lm (Yen et al., 1992), and trigger neural responses resulting in escape reactions. The consequence of small-scale turbulence is thus the enhancement of avoidance responses (escape reactions) to fluid deformations equivalent to those of a possible predator (Singarajah, 1975; Strickler, 1975a, 1977). Both the percentage of time allocated to slow swimming and the frequency of fast swimming (escape reactions) show a bell-shaped response to the intensity of small-scale turbulence (i.e., the rate of turbulent energy dissipation rate, e, L2 T 3). The optimum e value is species-specific and depends from the behavioural activity involved (MacKenzie et al., 1994; Caparroy et al., 1998). Moreover, there is a complex interaction between the food environment and the hydrodynamic motion in one side, and the balance between the energetic gains by the higher foraging efficiency and the losses due to the increase of escape reactions in the other (Costello et al., 1990; Marrase´ et al., 1990; Hwang et al., 1994; Alcaraz et al., 1994). In still (no turbulence) conditions and filtered seawater, tethered Centropages hamatus displays short burst of slow swimming and long breaks (Table 4). The fraction of time in slow swimming increases with food concentration and the contrary occurs with breaks, and interspersed are rare events of grooming and no escape reactions (Costello et al., 1990; Hwang et al., 1994). Turbulence represents a significant rise in the percentage of time spent in slow swimming either in filtered sea water or at low food concentration (Costello et al., 1990). The percentage of time in slow swimming increases by a factor of two, and is similar to that observed in calm Table 4 Effects of food type and concentration on the average velocity, duration of bouts and net-to-gross velocity ratio (2D and 3D tracking) during slow swimming, for Centropages typicus, C. velificatus and C. hamatus Species

Dimensions tracked

Food type and concentration

Centropages typicus Centropages hamatus Centropages velificatus Centropages velificatus Centropages velificatus

2D

Natural food**

1.9 (0.2)

2D

Natural food**

2D

Low food**

3D

Low food**

3D

High food

In parentheses standard deviation. ** Unknown food concentration.

Velocity (mm/s)

Net to gross velocity ratio (NGDR)

Authors

–

–

7.2 (2.7)

–

–

1.9 (0.7)

–

–

Tiselius and Jonsson (1990) Tiselius and Jonsson (1990) Bundy and Paffenho¨fer (1996) Bundy et al. (1993) Bundy et al. (1993)

16.5 (6) 6.3 (0.9)

Duration of swimming bouts (s)

21.9 (3.5)

0.24 (0.1)

47.6 (4.5)

0.18 (0.1)

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Table 5 Percentage of time allocated by Centropage hamatus to the different swimming activities under different conditions of small-scale turbulence and food concentration Turbulence conditions

Food conditions

Slow swimming

Breaks

Fast-swimming (escape responses)

Grooming

Pre-turbulence Turbulence Post-turbulence Pre-turbulence Turbulence Post-turbulence Pre-turbulence Turbulence Post-turbulence

Filtered sea water Filtered sea water Filtered sea water Low food concentration Low food concentration Low food concentration High food concentration High food concentration High food concentration

7.3 18.1 54.5 31.4 54.4 81.5 60.7 52.9 80.7

92.1 80.7 45.2 68.4 45 18.3 38.7 43.3 18.9

0.2 0.6 0.1 0 0.1 0 0.2 2.8 0.2

0.4 0.2 0.2 0.2 0.3 0.2 0.3 0.8 0.3

Modified from Costello et al. (1990).

% Time Slow Swimming

conditions under high food conditions (Table 4). At high food concentration, turbulence reduced the time spent in slow swimming. However, for C. typicus Saiz (1991) obtained different results, turbulence always resulting in a decrease in the time allocated to slow swimming. Differences in the experimental turbulence intensity could account for the discrepancies observed between both studies (see Table 5). Following the general rule described for other copepods, C. hamatus also increases the frequency of fast swimming (escape reactions) under turbulent conditions (Table 4). Costello et al. (1990), Saiz (1991), and Hwang et al. (1994) all described habituation effects to continuous turbulence (Fig. 6), so that under continuous stimulation there is a tendency for the frequency of escape reactions to decrease. This effect is crucial in terms of copepod social behaviour, in order to avoid the dispersion of copepod swarms (Hwang et al., 1994). The tendency to increase the frequency of escape reactions has important consequences for the energetic budget of copepods. The ratios between the energy costs derived from the whole swimming behaviour under turbulence and calm conditions are very much dependent on the food concentration. According to Marrase´ et al. (1990), in C. hamatus the ratios for the integrated swimming costs between turbulence and calm conditions, and for low food concentration (turbulence, low food/ calm, low food, TL/CL), range from negligible, to less than 0.5. However, at high food concentration the equivalent energetic ratios (TH/CH) range from 1.82

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Time (minute) Fig. 6. Time-course of the percentage of slow swimming (upper graph) and frequency of escape reactions (lower graph) for Centropages hamatus in alternate calm (NT) and turbulence (T) periods. See the habituation response of escape reactions. Re-drawn from Hwang et al. (1994).

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to 6.8. Moreover, at high food concentrations and turbulent conditions, the balance between the energetic gains derived from higher foraging efficiency, and the higher metabolic losses due to higher frequency of escape reactions, can be clearly negative (Saiz et al., 1992; Alcaraz et al., 1994). 5. Hydrodynamic and chemical cues: How to find a mate? The accurate perception of the surrounding world is probably the main reason for the success of copepods within marine ecosystems. Arrays of mechano- and chemoreceptors on the cephalic appendages (Strickler, 1975a; Barrientos, 1980) allow detection of the intensity and characteristics of hydrodynamic signals as well as identification of the trails of chemical exudates of other organisms. As seen above, the swimming patterns and the frequency and time allocated to the different behavioural components are modified by the abundance and characteristics of food particles, chemical trails and hydrodynamic disturbances (i.e., small-scale turbulence). The resulting behaviour under each condition depends on the trade-off between energy gains and losses (in the case of food encounters), as well as on the probability of being eaten or of finding a mate (in the case of hydrodynamic disturbances and chemical trails). To locate a co-specific individual of the opposite sex in a three-dimensional space, which may be thousands of body lengths away, would be quite improbable without clues or trails that could orientate the searching mate. The chemical sexual attractors (pheromones, Katona, 1973) are dispersed by females and detected by males displaying an amazingly complex behaviour. Sometimes females, when detecting male exudates, react by changing the smooth gliding by hops, like in Temora longicornis (Van Duren et al., 1998). This behaviour enables ephemeral but strong hydrodynamic signals to increase the encounter probability with female trails while males swim in sinuous paths. Chemical attractors or pheromones are probably aminoacids, relatively cheap to release from an energetic point of view (Bagøien and Kiørboe, 2005). They seem to be also relatively unspecific, as T. longicornis males sometimes track other male’s trail as well as their own (Doall et al., 1998). In some cases, females lay vertical trails that are searched by males swimming in horizontal trajectories (Calanus marshallae, Tsuda and Miller, 1998), while in others there is no preferred direction (Temora stylifera, Doall et al., 1998). In general, males display swimming behaviours that enhance the probability of crossing the pheromone trail of a female. In the case of Centropages typicus (Bagøien and Kiørboe, 2005), the probability of detecting a female trail is inversely proportional to the trail length and age. C. typicus can successfully track trails 10 seconds old which are very convoluted and as long as 17 cm (Fig. 7). In this case the chasing behaviour of males includes rapid changes in velocity and direction, sometimes retracing the way if the direction followed is the wrong one. The swimming speed of C. typicus when looking for female trails can increase by a factor of 5 in comparison to slow-swimming, and further increases to a factor of 15 when following the path. If the trail is lost, there is a sudden change in direction and a new velocity increase up to 70 mm/ s, a 30-fold increase from the normal, slow-swimming speed (Tiselius and Jonsson, 1990; Bagøien and Kiørboe, 2005). 6. Light-related effects on Centropages swimming behaviour Generally, the frequency and percentage of time allocated to the different components of copepod motion are in part related to daily rhythms of feeding activity, the photo-responsive behaviour depending on the wavelength of the light. The range of spectral sensitivity and the irradiance intensity threshold vary between species, and strongly modulate most of the components of copepod activity (swimming velocity and path shape, escape reactions, vertical migration, etc., Cohen and Forward, 2002) and their ecological consequences. Species distributed during daylight hours in relatively deep layers and displaying diurnal rhythms (i.e., in feeding, swimming, etc.) generally respond to a narrow range of wavelengths, their activity spectrum generally matching the ambient light during the time of undergoing the activity (Forward, 1988). On the contrary, surface dwelling species, with non-defined daily rhythms, are sensitive to a broad range of wavelengths (Cohen and Forward, 2002). Centropages typicus displays a characteristic day-night feeding rhythm (Calbet et al., 1999), and during daylight hours remains in relatively deep layers (Saiz and Alcaraz, 1990). When chemical, biological or physical stimuli do not interfere with light conditions (i.e., in the absence of chemical- or biologically active molecules,

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Time (1/25 s) Fig. 7. Example of swimming behaviour of male (grey dots) Centropages typicus when crossing the pheromone trail of a female (black dots, 3D swimming tracks). The male intercepts a 23 s old pheromone trail of a female, tracks it in the wrong direction, corrects and then encounters the female at E. Points separated by 1/25 s. After Bagøien and Kiørboe (2005).

food particles, or hydrodynamic motion), the spectral sensitivity is reduced to a quite narrow band of the spectrum, between 480 and 560 nm, with a peak at 500 nm. Between these wavelengths, light intensities as low as 0.7–1 · 1013 photons m 2 s 1 can elicit photo responses (Buskey et al., 1987). The swimming pattern in darkness, typically a hop and sink motion, distinctly changes to linear swimming when stimulated by light. Another aspect of copepod swimming behaviour related to environmental irradiance conditions is the photonegative response of Centropages, as occurs in other copepod species, to sudden changes in light intensity. It generally consists in a sudden increase in the swimming speed, and in the number and duration of fast-swimming bursts and escape reactions (Buskey et al., 1987; Buskey and Swift, 1983). 7. Vertical migration: the compromise between eat and to be eaten Although in some circumstances Centropages appears as a non-migrating genus (Sameoto, 1984; Turner and Dagg, 1983), most frequently is observed to perform a normal, nocturnal upward motion to surface waters followed by diurnal descent or vertical dispersion at night. The possible control of vertical migration by predation is supported by data on long-term changes (37 years) in night-day abundances (the N/Dindex, Hays et al., 1996) of the continuous plankton recorder samples. The abundance of planktivorous fish would determine changes in the N/Dindex. For example, for Centropages typicus, there is a negative correlation between the N/Dindex and herring abundance, whereas for C. hamatus the correlation coefficient is positive. This has been explained as the consequence of size-dependent differences in their vertical migration range (Hays et al., 1996). The maintenance of the vertical migration patterns of adult C. typicus in oligotrophic, density stratified areas (Fig. 8), with almost no phytoplankton food in surface waters and a well developed deep phytoplankton layer, could seem energetically inefficient. Tentatively, the behavioural and trophic plasticity of C. typicus would allow feeding during the day in the deep phytoplankton layer, and during the night to prey on surface,

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Fig. 8. Vertical migration of Centropages typicus. Changes along 24 h in the vertical distribution of adults during the summer stratification period in the Catalan Sea (NW Mediterranean). The shadowed area indicates the night hours. Dashed line shows the position of the centre of gravity of the population. Modified from Saiz and Alcaraz (1990).

non- autotrophic organisms (i.e., ciliates), changing the feeding mode from suspension- to ambush feeder. On the other side, the ascent at night to surface water, poor in nutrients and autotrophic food, will result in a reversal of the normal active vertical transport of matter. C. typicus (and all zooplankton migrators in oligotrophic, density stratified areas) would behave thus as ‘‘prudent predators’’ (Margalef, 1974), counteracting the downward transport of nutrients contained in settling phytoplankton cells and faecal pellets. This active upward transport would represent nutrient inputs that could result in the enhancement of primary production in the mixing layer, above the nutricline (Alcaraz, 1988; Saiz and Alcaraz, 1990), with significant consequences for shaping the structure and function of planktonic systems. 8. Conclusions The behaviour of Centropages, as in all copepods, is tightly linked to, and depends on, all the remaining aspects of their biology, from feeding and searching for mates, to avoiding predators. This behaviour changes significantly during the organism’s development, the complexity of the motion pattern increasing after the last naupliar stage. For late copepodites and adults, the response of Centropages swimming pattern to changes in most environmental factors does not differ essentially from the response observed in other calanoids. Food concentration and quality modify the swimming mode and velocity (i.e., when shifting from cruising to ambush mode), and the reaction to turbulence can be more or less pronounced, but always resulting in an increase of the frequency of fast swimming (escape reactions). Vertical migration, a widespread behaviour controlled by swimming characteristics (velocity and direction) only differs from other migrating Calanoids in details related to possible lags in the starting time of the ascent, and on its vertical extent. However, in the aspects related to reproduction the swimming behaviour of Centropages shows a significant degree of specificity. The necessity for accurate identification of hydrodynamic signals is imperative, the confusion between a predators’ trail and that of a conspecific of the opposite sex being fatal. For this reason, the swimming involving mate searching is usually the most highly specific (even sex-specific) of all the copepod’s behaviour. The process of tracking trails, finding and following them, possible courtships, mating, etc., appears to be the most complex swimming behaviour. In summary, the different motion patterns displayed by copepods of the genus Centropages and the rich repertoire of strategies allocated to the different vital activities explain their considerable success in exploiting marine planktonic environments. Further efforts addressed towards the study and modelling of the control exerted by microscale biological, chemical and physical signals (i.e., fine layering and micro-heterogeneities of temperature, salinity, light transmission, phytoplankton, shear, etc.) on Centropages behaviour, patchiness, ontogenic spatial segregation and dynamics, will surely contribute to a better understanding of the role in pelagic systems of the genus in particular and of copepods in general. Acknowledgements This work was supported by Grants REN2001-1693, (ZOOTRANSFER) to E. Saiz, CTM2004-02757/ MAR (MICROROL) to A. Calbet, and REN2002-04151-C02-C01 (EFLUBIO) to M. Latasa. A.C. was

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