Atlantic and in the Arctic (Rose, 1933; Grice, 1962). Its ...... London: Allen and Unwin 1966. George ... Grice, G. D.: Copepods collected by the nuclear submarine.
Marine
Marine Biology94, 347-356 (1987)
::=:-=-Biology
9 Springer-Verlag 1987
Temperature and plankton II. Effect on respiration and swimming activity in copepods from the Greenland Sea H.-J. H i r c h e AIfred-Wegener-Institut for Polar- und Meeresforschung; Columbusstral~e, D-2850 Bremerhaven, Federal Republic of Germany
Abstract
The relationship between temperature and metabolism was studied in Arctic copepods with regard to the concept of metabolic cold adaptation of polar poikilotherms. Temperature tolerance and respiration rates of the dominant copepods Calanus finmarchicus (Gunnerus), C. glacialis (Jaschnov), C. hyperboreus (Kroyer) and Metridia longa (Lubbeck), collected in Fram Strait, Greenland Sea, in July 1983, were studied at different temperatures. Temperature tolerance in the boreal C.finmarchicus was slightly higher than in the three Arctic species. Respiration rates at lower temperatures followed the Arrhenius equation in all species, with values for ~ (temperature characteristics) between 11.05 and 22.95, corresponding to a Q10 between 2.05 and 4,5. This increase in metabolic rate with rising temperature was not related to an increase of swimming activity, as was shown by videoanalysis. "Activity" was determined as average swimming speed and as frequency of certain locomotor patterns. Average swimming speed remained unchanged at all temperatures and was ca 1 cm s -1 for all species, when only periods of active swimming were considered. The time spent with active swimming did not change with temperature in M. longa and C.finmarchicus, but decreased in C. glacialis. In C. hyperboreus it increased at 5 ~ and decreased again at higher temperatures. It is suggested that the increase in oxygen consumption is fully accounted for by the basal metabolism.
arctic, but not for Arctic poikilotherms. Results from metabolic measurements on Antarctic zooplankton did not support this concept (Hirche, 1984). According to Clarke (1983), it is the basal metabolism that is critical to any discussion of metabolic cold adaptation, for it is this, rather than the cost of feeding, growth or activity, that is believed to be elevated. The total oxygen consumption of an aquatic poikilotherm is the sum of a basal (standard) metabolism and additional consumption, attributable to physiological processes other than subsistence (Prosser, 1973). Among the latter, the demand for energy by locomotion is the most important (Brett, 1972). Increased swimming activity has been shown to triple the metabolic rate of pelagic crustaceans (Ivlev, 1963; Mickel and Childress, 1978) and to raise that of fishes by as much as an order of magnitude (Fry, 1971). According to Halcrow and Boyd (1967), the influence of temperature on metabolism is to a large extent an expression of changed locomotory activity. Measurements of temperature sensitivity of metabolism in spontaneously active animals (i.e. the "routine" rate of Fry, 1957) are of limited comparative value without additional information on the activity accompanying the metabolic rate. No measurements on the activity of copepods and its influence on their metabolic rate have been reported in the literature, nor has the influence of temperature on copepod activity been studied so far. This study focusses on the potential contribution of swimming activity to total metabolism at different temperatures by concurrently measuring respiration and activity in parallel experiments. The frequency of locomotor patterns and swimming speed, as determined by videoanalysis, were taken as indicators for activity.
Introduction
This work is part of a comparative study in which the relationship between temperature and metabolism in polar zooplankton is being examined (Hirche, 1984). It focusses on the concept of metabolic cold adaptation as presented by De Vries (1977) and George (1977). This concept comprises elevated metabolic rates, obligate stenothermy, and the loss of genetic acclimatization potential for Ant-
Materials and methods
Species examined The four copepod species examined were Calanus finmarchicus (Gunnerus), C. glacialis (Jaschnov), C. hyperboreus (Kroyer) and Metridia longa (Lubbock).
348
H.-J. Hirche: Respiration and swimming activity in copepods
Calanus finmarchieus is one of the most abundant copepods in the North Atlantic (Fleminger and Htilsemann, 1977). According to Jaschnov (1970), its area of reproduction lies in the two great cyclonic gyres situated in the northern part of the North Atlantic and in the Greenland and Norwegian seas. Calanus glacialis is a widespread species in the Polar Basin and in the Arctic Seas. From there it is carried out into the northern areas of the Atlantic and Pacific Oceans by cold currents. The southern boundary of its range extends along the Polar Front (Jaschnov, 1970; Fleminger and Ht~lsemann, 1977). Calanus hyperboreus is a typical Arctic species occurring in all Arctic seas (Brodsky, 1967) and in the North Atlantic. Persistent stocks occur in the deep stagnant layers along the Norwegian coast and in deep Norwegian fjords (Wiborg, 1954; Matthews et al., 1978). Metridia longa is an abundant species in the North Atlantic and in the Arctic (Rose, 1933; Grice, 1962). Its distribution is similar to that of Calanus hyperboreus.
Collection of material The copepods were collected during the PRE-MIZEX cruise of RV "Polarstern" in July 1983 in the Greenland Sea. Live copepods were caught with a bongo net (300and 500-~m mesh size). Closed 2-liter jars served as cod ends to avoid damage to the material. The net was veered obliquely at 0.5 m s -1 to 100 m depth and hauled at the ship's speed of 0.5 knots. The catch was immediately diluted with surface water. The whole catching procedure usually did not exceed 10 min.
Experiments Individual copepods were sorted immediately after sampling, identified under the microscope, and transferred into the experimental containers. Details of collection, environmental temperatures and experimental procedures are given in Tables 1 and 2. For temperature tolerance experiments, copepods were placed in 60-ml glass bottles containing filtered seawater (0:8/zm G F / C ) at ambient temperature. The bottles were incubated in a temperature gradient bloc at temperatures from -1.8 ~ to 25 ~ and were kept in the dark. The highest temperature was reached in the bottle after 30 rain. After 24 h the copepods were checked for survival under a dissecting microscope. For respiration experiments, copepods were placed in 60-ml bottles containing aerated filtered seawater at experimental temperatures. The oxygen content of each bottle was measured before and after incubation using a Radiometer oxygen probe. The bottles were placed in the temperature gradient bloc together with blanks at each temperature. Light intensity at the surface of the bottles was 4 r a fluorescent lamp served as light source. Incubation time was adjusted so that AO~ during the experiment never exceeded 10%. Experimental copepods were rinsed with distilled water, stored at -20 ~ for transport to the laboratory, later dried to constant weight at 70 ~ and weighed. For analysis of the swimming activity, ten Metridia longa females, ten Calanusfinrnarchicus females, eight C. glacialis CV and six C. hyperboreus females, respectively, were placed in crystal glass cuvettes of 1 0 x l 0 x 5 c m containing 320 ml of filtered seawater (0.8/~m GF/C) and
Table 1. Calanus spp. and Metridia longa. Sampling locations for temperature tolerance tests Species
C.finmamhicus Cfinmarchicus C hyperboreus C. hyperboreus C glacialis M. longa
CV CV
~? CV CV ?
Date 1983
Location (Lat.-Long.)
Temp. (~ surface-100 m
Copepods No. of experiments per bottle
July 3 July 13 July 25 July 25 July 6 July 13
68~176 12'E 79~176 80~19'N-01 ~ 80~19'N-01~ 75~176 79~176
9.0-6.7 2.0-2.2 0 -3.9 0 -3.9 3.1-1.4 2.0-2.2
4 4 8 8 8 4
8 8 2 3 3 7
Table 2. Calanus spp. and Metridia longa. Sampling locations and details of respiration experiments Species
Cfinmarchicus C. hyperboreus C. hyperboreus C. glacialis M. longa
?_ ? CV CV ~
Date 1983
Location
July 17 July 17 July 15 July21 July 11
79~176 79~ 79~176 79~176 79~176
~17'E
Temp. (~ Time surface-100 m (h)
Copepods Dry wt per ~g/ind.) bottle
- 1.7-(+4.2) - 0 . 5 - ( - 1.7) - 0 . 7 - ( - 1.7) 2.7-3.1 2.0-2.2
3-5 2-3 3-5 3-5 3-5
12 10 8 12 12
0.326 2.087 2.412 0.560 0.302
H.-J. Hirche: Respiration and swimming activity in copepods held in modified refrigerators at 0 ~ 5 ~ 10~ and 15 ~ (+ 0.5 C~ The copepods were from the same haul as those used in respiration experiments and both experiments were run concurrently. The refrigerators were illuminated from above; irradiance was 4 p E m -2 s-1 at the level of the cuvettes. After 4 h of acclimation, the copepods were filmed with a Panasonic WV 3890E videocamera over a period of ca 30 rain at each temperature through a window in the front door. The videotapes were analysed for locomotor patterns and swimming speeds, using a Panasonic videorecorder NV8505 with a single frame counter and a Sony PVM 1370Q superfine pitch monitor. To calculate swimming speeds, the coordinates of copepods were determined on a transparent mm-grid mounted on the monitor screen. Swimming distance was then divided by the number of frames obtained with the frame counter.
Results
Temperature tolerance The results of the temperature tolerance tests are shown in Fig. 1. All copepods survived temperatures up to 12~ Above 15 ~ individuals of Calanus glacialis and Calanus hyperboreus were torpid and floated motionlessly in the water. Even gentle touches with a forceps did not activate them. However, their hearts were clearly beating indicating that they were still alive. In accordance with their widespread geographical distribution, Calanus finmarchicus showed the highest temperature tolerance. Different environmental temperatures at the two sampling locations had only little effect on their temperature tolerance. Lowest temperature tolerance was found in CV and females of Calanus hyperboreus, whereas C. glacialis and Metridia longa exhibited a rather similar tolerance which lay between C. hyperboreus and C. finmarchicus.
349 Respiration When the reciprocal temperatures, expressed in degrees of Kelvin, are plotted against the logarithms of the respiration rates, the dependence of respiration on temperature can be represented satisfactorily by the Arrhenius equation in the form of a straight line V-- V e e ~IRT,
where V is the respiratory rate, V0 is a coefficient having the same units as V,/~ is the "temperature characteristic", i.e. the coefficient expressing the accelerative influence of temperature, R is the gas constant (1.987 kcal mo1-1) and T is the absolute temperature (K). In all species, respiration rates followed the Arrhenius equation, at least at the lower temperatures (Fig. 2). Respiration rate in Calanus glacialis reached a plateau at about 10~ In Metridia longa, respiration decreased above 11 ~ For comparison, literature data for C. hyperboreus (Conover, 1962), 34. longa (Haq, 1967) and C. finmarchicus (Marshal et aI., 1935) are induded in the plots of Fig. 2; for details see figure caption, These data also fit the Arrhenius equation (Table 3). The M. longa of Haq (1967) attained their maximum respiration rate at 14~ which is 3C ~ higher than in the present experiments. The Q10 calculated for a temperature range between 0 ~ and 5 ~ and 5 ~ and 10~ together with the coefficients for the Arrhenius equation, are listed in Table 3. The data obtained can be divided into three groups: Calanus glacial& with the highest temperature characteristic, C. finmarchicus with an intermediate and both stages of C. hyperboreus and Metridia longa with the lowest values. The coefficients a and b of the last group are not significantly different at the 5 % level.
Swimming activity
Loeomotor patterns 100
/ID/....M3~:
*C, Hnmsrchicus CVI
..... h,cu cv @C.hyperboreus s
c,, -~
X C.gloclalis CV
4b
//
/
y
//
/ / / /
/ / //
]
/ / *
Jo Temperature (~
25
Fig. 1. Temperature tolerance of four Arctic copepods. Calanus
flnmarchicus I =July 3, II =July 13 (see Table 1)
Swimming tracks of the four species investigated at 0~ are shown in Fig. 3. The registration period was chosen randomly. For Calanus finmarchicus and C. glacialis some of the tracks were shifted horizontally to avoid overlapping. The tracks may be grouped into three categories according to differences in patterns and in activity: C. glacialis and C. finmarchicus with a similar pattern but with C. glacialis more active; C. hyperboreus showing very little activity and no characteristic patterns; and Metridia longa showing high activity and a characteristic pattern. In order to quantify the behaviour of the different species and to measure the activity, only swimming patterns which appeared typical were selected, i.e. those that occurred frequently and could be recognized even when variations were superimposed.
350
H,-J.Hirche: Respiration and swimming activity in copepods Temperature 0
1,0
5
I
10
J
I
0,5-
15
20
'
'
o
(~ 0l
1.0"
5I
10 I
15 I
20 I
015-
j
0-
0-
-0,5-
-0.5-
o o
-1.0-
o /
-1.0-
o
9 /9 f
-1.5-
"
o
-1,5-
o
Calanus hyperboreus r
37
t-" i
0-
O~
-0.5E
-1.0 -
e"-
-1,5t,'o
o
"Js
5
I
1.0-
"7
"0
i
J6 0
A
Ca/anus hyperboreus CV
i
37
10
I
15
I
/
20
I
o
I
0
5
I
1.0-
I
0.5-
B
o
36 '
'
o
15
I
I
3/. ' 20 I
.g -0,5-
/,
-1.0-
-1,5-
Ca/anus g/acialis CV
Metridia /onga
'
37
"Js
'
37
6 Temperat
5
I
1.5"
10
'
0-
/o 0
e'l
3"5
/ /
8
o o
'
10
I
15
I
5
ure
3/,
(I/K XI0-3)
20
I
"/
I
1.0 n," o.J i-
f
9
/
9
o
o
o
o
0-
:o
-0,5-
Fig. 2. Arrhenius plots for respiration rates of four Arctic copepods. Filled circles: Calanus hyperboreus CV=Conover (1962) his Fig. 3, assuming dry weight of 2 mg copepod-1; C finmarchicus = Marshall et al. (1935), assuming dry weight of 200/zg; Metridia longa=Haq (1967), his Fig. 1, assuming dry weight of 300 Hg
-1.0-
-1,5Calanus fl)~marchtcus
3.7
'
~6
'
Temperature
~.5
'
3'.~
( 1/K X10-3)
The following patterns were classified in the Calanus species (Table 4): Hop-and-sink swimming (HS), as represented by a sawtooth like swimming track (Fig. 3), is the most characteristic swimming pattern of Calanus finmarchicus
(Lowndes, 1936; Bainbridge, 1952) and C. glacialis. Especially in C.finmarchicus the HS was often performed directly above the bottom of the aquarium (see Fig. 3 a). Sinking was then interrupted regularly when the copepod touched the ground, and another hop followed immediately. In its extreme, copepods lying
H.-J. Hirche: Respiration and swimming activity in copepods a
351
I
9
\
c
s2
.1~ ~
o----,
Fig. 3. Swimming tracks of four Arctic copepods. (a) Calanusfinmarchkus: 10 individuals, 60 s; (b) C glacialis: 10 individuals, 30 s; (c) C hyperboreus: 6 individuals, 60 s; (d) Metridia longa: 5 individuals, 30 s (Marks on tracks of C. hyperboreus: every 2 s; numbers on tracks: seconds since start). Open circles: start; closed circles: end of observations; asterisk: no locomotion during observation period
Table 3. Calanus spp. and Metridia longa. Coefficients of Arrhenius equations, correlation coefficients and Q10.-: no data Species
a
b
r
kt
Q10
Reference
0o_5oc
5o_10oc
C.finmarchicus C.finmarchicus
? ~
33.31 16.53
- 9.34 0.96 - 4.45 -
18.55 8.84*
3.44 -
3.31 -
C hyperboreus' C. hyperboreus C. hyperboreus C. glacialis M. longa M. longa
~ CV CV CV 2
23.59 20.74 15.40 41.20 20.21 27.15
-
13.45 11.90 9.18 22.94 11.04 15.15
2.44 2.22 4.60 2.09 -
2.38 2.15 4.39 2.04 -
6.77 0.98 5.99 0.98 4.62 11.55 0 . 9 7 5.56 0.98 7.63 -
This study Marshall et aL (1935) This study This study Conover (1962) This study This study Haq (1967)
* Assuming dw = 200/~g copepod -1
on the ground were " b o u n c i n g " gently on their tails with the body pointing more or less vertically upwards, as already described by Harris (1963). "Jumps" were movements significantly faster than o t h e r swimming patterns a n d always i n c l u d e d a n t e n n u l e strokes. Sometimes j u m p s Originated in collisions with other individuals (ca 20%), b u t mostly no external trigger was observed. For analysis, a j u m p ended when no more significant locomotion was observed a n d the a n t e n n u l e s were b e i n g stretched out again. E x a m i n a tion of m a n y j u m p s of Calanus hyperboreus suggest that, during the j u m p , the a n t e n n u l e s were w o u n d
-
-
-
around the body a n d beat flagellum-like, thus contributing to propulsion. All other active patterns were l u m p e d as "other" patterns. Amongst these is a looping-like pattern which was observed regularly in Calanusfinmarchicus and C. glacialis (Fig. 3 a, b). Long phases of immobility were observed in all Calanus species. N o n - m o b i l e copepods in the water c o l u m n and those on the bottom were distinguished. Copepods which moved their bodies, but did not show measurable locomotion, were also registered. Individuals lying on the bottom often moved the thorax up and
352
H,-J. Hirche: Respiration and swimming activity in copepods
Table 4. Calanus spp. and Metridia longa. Frequency (%) of locomotor patterns of four Arctic copepods at four temperatures. H = Hop; J = Jump; S = Sinking; B = bottom lying; M = non-mobile; L = movements without locomotion. For details see text. -: not observed Temp. (~
C.finmarchicus
J
other
S
B
M
5 10 15
47.6 39.4 20.7 21.8
0.3 0.3 0.3 0.4
3.3 18.9 11.0 12.9
37.8 43.4 19.8 19.7
26.0 23.8 43.8 31.3
10.6 8.1 8.9 23.2
5.3 1.5 6.6
14.1 16.1 3.2 15.9
CV
0 5 10 15
56.1 56.1 18.4 15.3
1.1 0.9 1.6 1.8
26.9 17.6 17.0 15.4
36.7 42.1 14.6 15.0
3.5 7.3 40.9 41.9
10.9 17.8 18.7 1.8
1.2 0.3 4.2 25.4
47.7 32.5 21.6 15.9
~
0 5 10 15
-
0.4 0.7 0.4 0.5
1.2 2.0 1.3 0.9
-
2.7 2.7 10.4 15.9
95.9 94.7 87.9 82.6
-
1.6 2.7 1.7 1.4
7
0 5 10 15
4.5 4.4 8.7 5.1
45.2 47.2 40.4 51.0
-
-
2.4 1.6 5.8 4.7
-
97.6 98.4 94.2 95.3
?
0
(n=36 000 frames)
C. hyperboreus (n = 675 000 frames)
Metridia longa (n= 15 000 frames)
27 active
HS (n =45 000 frames)
C. glacialis
Inactive
Active
47.9* 46.8* 45.1" 39.2*
L
* Screw-like swimming
9 C.FINMARCHICUS 80
,
C.GLACIAUS
9o
METRIDALONGA
l l ]~
ITII Activity and temperature
6O
g
~
5
9 40-
2O
0
tact and collisions with other individuals usually resulted in jumps. After touching the water surface, a reverse j u m p followed (see Fig. 3 d).
S I5 ~ ' ~ ~15 ~
y = 0.029+ 1.050x R = 0.99 20
40
60
SWIMMING TIME (s) Fig. 4. Relationship between time of active swimming and swimming distance of four Arctic copepods. Bars represent standard deviations; numbers indicate experimental temperatures for
CaIanus glacialis
down rhythmically like a r u d i m e n t a r y HS. In other cases, copepods r e p e a t e d l y b o u n c e d with their h e a d s against the b o t t o m or the a q u a r i u m wall. In contrast to the Calanus species, Metridia longa swims almost permanently. Its swimming is best described as a smooth gliding. A frequent pattern is the swimming in horizontal circles o f almost constant diameter. Wall con-
The frequency o f locomotor patterns shows a strong effect o f temperature on both the b e h a v i o u r and the activity o f the three Calanus species (Table 4). Some behavioural changes show the same trend in several species. Thus the typical HS pattern o f C.finmarehicus and C. glaeiaIis is reduced a b r u p t l y between 5 ~ a n d 10~ in both species, while it remains almost constant at the lower temperatures. "Bottom-lying" in these species increased m a r k e d l y between 5 ~ a n d 10 ~ In all Calanus species the ratio o f " b o t t o m - l y i n g " to " i m m o b i l i t y " changed with temperature. The frequency o f " n o n - l o c o m o t o r " pattern in C. glacialis at 15 ~ was r e m a r k a b l y high. I n contrast, the b e h a v i o u r ofMetridia longa appears unaffected by temperature. Activity was calculated as the time spent i n forward swimming. In contrast to Lowndes (1935), but in agreem e n t with Robertson and Frost (1977), no active movements o f swimming a p p e n d a g e s during the sinking period were observed. Activity r e m a i n e d constant at all temperatures, except for Calanus glaciaIis, where it decreased continuously with rising temperature. The distance o f the swimming track over time was used to calculate the average swimming speed. Only active swimming was considered and sinking distance was neglected. W h e n average distance is plotted against active swimming time at all four temperatures, a linear regression is o b t a i n e d ( r = 0 . 9 9 ) (Fig. 4). This indicates that, at all t e m p e r a t u r e s studied, average swimming speed is ap-
H.-J.Hirche: Respiration and swimming activity in copepods proximately the same (1 cm s -1) for all species. The figure also shows that there is no clear trend of activity/average swimming speed and temperature, except for Calanus glacialis, where an inverse linear relationship was seen.
Discussion
Temperature tolerance Results of temperature tolerance experiments reported here are in agreement with those of De Vries (1977) and George (1977) insofar as the Arctic species did not show stenothermy. However, the Antarctic copepod species Euchaeta antarctica and Calanoides acutus did not show stenothermy either (Hirche, 1984), although it has been postulated for Antarctic invertebrates according to the concept of metabolic cold adaptation represented by the above mentioned authors. Temperature tolerance of the three species restricted to Arctic water masses was somewhat lower (15 ~ to 20~ than that of the boreal Calanus finmarchicus (slightly above 20~ According to Marshall and Orr (1972), C.finmarchicus is found at temperatures b e t w e e n - 2 ~ and 22 ~ Their data, however, also include CaIanus helgolandicus, the warmth-loving southerly form. In respiration experiments by Anraku (1964), all C.finmarchicus died at 22.5 ~ whereas all survived temperatures of 15 ~ No information was found on the temperature tolerance of Calanus hyperboreus and C. glacialis. In the Gulf of Maine the range of temperatures in which C. hyperboreus normally lives varies from 2 ~ to 8 ~ (Conover and Corner, 1968). McLaren etal. (1969) reported successful hatching of C. gIacialis eggs at temperatures from 0 ~ to 7.9 ~ Metridia longa has a geographic distribution similar to CaIanus hyperboreus. In his respiration experiments, Haq (1967) found that at 18 ~ all his copepods died within 12 to 18 h, whereas in this study most were still alive at 18 ~ after 24 h.
Respiration Respiration rates measured here were comparable to those found by other authors (Table 5). A comparison is often difficult due to lack of information on developmental stage or incubation temperature. For comparative data on Calanusfinmarchicus, see Marshall and Orr (1973). The respiration rates measured represent a direct response of metabolism to different temperatures. As was found in Antarctic zooplankton (Hirche, 1984), respiration in all species and stages from the Arctic also followed the Arrhenius equation. This also applies to the literature data included in Fig. 2. Ivleva (1973) took this as an indication for full acclimation. In two species, respiration reached a plateau or decreased, respectively, at higher temperatures (ca 10 ~ in
353
CaIanus glacialis and 12~ in Metridia longa). These temperatures are well below the range of these species, as was shown by temperature tolerance tests. The two species are therefore apparently capable of regulating their metabolism well in advance of lethal temperatures. The temperature characteristics of the Arrhenius equations of the Antarctic copepods Euchaeta antarctica and Calanoides acutus (23.84 and 21.24, respectively, Hirche, 1984) were at the higher end of the range found here for the Arctic species (11.04 to 22.94). However, temperature response of metabolism showed seasonal variability related to physiological condition in Calanus finmarchicus and C. helgolandicus (Hirche, 1983), and seasonal changes in Q10 (measured between 2 ~ and 8 ~ of respiration rate from 17.6 to 4.2 in August were reported by Anraku (1964) in C. finmarchicus. Metabolic responses to acute temperature changes were similar in the Arctic and Antarctic copepods compared here, showing no indication of metabolic cold adaptation for the Antarctic species.
Swimming behaviour Studies on the behaviour of small planktonic organisms such as copepods, using optical methods, require relatively small aquaria for them to remain in focus and to obtain a sufficiently high resolution. For metabolic rate measurements, experimental volume also has to be restrained, due to sensor resolution or analytical sensitivity. Consequently, limited space and frequent wall contact, together with light refractions and crowdedness, may disturb natural behaviour and metabolism. Pavlova (1977) found an increase in total locomotor activity and respiration rate with increasing volume of the aquaria. However, direct insitu observation (Bainbridge, 1952) or the sophisticated field-simulating system of Hardy and Bainbridge (1954) cannot be used for comparative studies of physiological rate measurements and swimming activities under similar conditions. The behaviour of Calanus finmarchicus and C. glacialis at environmental temperature was consistent with actual underwater observations on Calanus species near the surface (upper 30cm) by Bainbridge (1952). He observed the copepods to hop and sink, and to be intercepted by occasional darts and a good deal of horizontal movement. However, the high proportion of bottom-lying individuals of all the Calanus species is a clear indicator of unnatural behaviour due to laboratory conditions. The question arises as to whether the inactivity of C. hyperboreus, and to a lesser degree that of the other two Calanus species, reflects starvation conditions during the experiments and/or limited food conditions in the sea during sampling. Chlorophyll a concentrations at the sampling site were very low (0.13 mg m -3 in the upper 50 m; J. Lenz, University of Kiel, personal communication). Williamson (1981) reported a pronounced difference in the swimming behaviour of Mesocyclops edax in high and low prey densities. Centropages typicus spent less time in slow
354
H.-J. ttirche: Respiration and swimming activity in copepods
Table 5. Calanus spp. and Metridia longa. Respiration rates from the literature and the present experiments Species
Stage
Locality
(1) C.finmarchicus
~
Fram Strait Fram Strait Fram Strait Fram Strait Fram Strait Fram Strait
(2) C. glacialis
?
Gulf of Maine
CV
Fram Strait Fram Strait Fram Strait Fram Strait Fram Strait Fram Strait Fram Strait
(3) C. hyperboreus
0 3.0 6.0 9.3 15.1 17.9 4-6 0 3.2 6.2 9.0 11.7 14.5 17.3
SD
n
Reference
0.454 0.502 0.830 1.353 1.983 3.840
0.150 0.183 0.124 0.097 0.627 0
3 3 3 3 3 2
This study
1.04-1.96 0.329 0.534 0.789 . 1.300 1.184 1.394 1.467
Conover and Corner (1968) 0.075 0.051 0.065 0.273 0.157 0.079 0.318
3 3 3 3 3 2 3
This study
CIV+ CV+ $
W. Spitsbergen Barents Sea
CV
Gulf of Maine Gulf of Maine
CV ?
Gulf of Maine Gulf of Maine
?
Swedish west coast
5-6
0.14-0.41
Bgtmstedt (1979)
Swedish west coast Fram Strait Fram Strait Fram Strait Fram Strait Fram Strait Fram Strait Fram Strait
? - 0.8 1.2 4.9 7.7 10.7 13.6 17.1
0.14-0.49 0.300 0.346 0.383 0.534 0.791 0.987 1.319
0.092 0.144 0.072 0.047 0.162 0.330 0.041
4 4 3 4 4 4 4
Bgtmstedt (1983) This study
Fram Strait Fram Strait Fram Strait Fram Strait Fram Strait Fram Strait
- 0.5 3.5 6.5 9.1 12.2 14.6
0.308 0.361 0.520 0.633 0.761 0.942
0.038 0.027 0.056 0.055 0.101 0.023
3 3 3 3 3 2
CV
9 ?
Gulf of Maine
?
Respiration /tl 02 mg dw-~ h-1
CV
?
(4) 34. longa
Temp. (~
- 1.8 10 4-6
0.29-0.39
Bgtmstedt (1984)
0.2-0.8
Bgtrnstedt and Tande (1985)
0.49 0.23-0.30
Conover (1960)
0.30-0.63 0.32-0.57
0.5-0.6
Conover and Corner (1968)
This study
5-6
1.13
B~tmstedt (1979)
4-6
0.63-1.96
Conover and Corner (1968)
?
Gulf of Maine
5
0.55 - 1.28
Haq (1967)
?
Swedish west coast
?
0.77-1.57
B~tmstedt (1983)
?
Fram Strait Fram Strait Fram Strait Fram Strait Fram Strait Fram Strait
- 1.6 2.0 6.0 8.9 11.5 15.9
swimming mode and more time at rest as food concentrations decreased (CoMes a n d Strickler, 1983). The p e r m a n e n t "gliding" of Metridia species was reported ealier by Sars (1903). It is not clear, however, whether this pattern reflects feeding or starvation. A comparison of data on swimming speeds with data from the literature is only possible for Calanus finmarchicus a n d Metridia pacifica. Hardy a n d Bainbridge
0.807 0.918 1.410 1.648 1.981 1.830
0.035 0.045 0.066 0.014 0.146 0.077
2 2 2 2 2 2
This study
(1954) reported a speed of 1.83 cm s =1 for upward swimming and 2.97 cm s -1 for active downward swimming over a period of 2 m i n in C.finmarchicus. This is remarkably faster than the average speed found in this study (ca 1 cm s-l). From the vertical distribution at close sampling intervals, Enright (1977) calculated the upward swimming speed for M. 1)acifica to be 2.5 cm s-L This is higher than the average speed found here, even if one takes into
H.-J. Hirche: Respiration and swimming activity in copepods account underestimation due to two-dimensional projection.
Activity and metabolism The activity of poikilotherms, and hence their metabolism, usually increases with temperature (Laudien, 1973). An increase in the frequency of limb beat by barnacle nauplii was found by Yule (1984). The cruising speed of Cyclops strenuus changed from 0.39 cm s -1 at 7~ to 0.55 cm s -1 at 25 ~ (Rosenthal, 1972). Halcrow and Boyd (1967) studied the influence of temperature on both the standard and the routine metabolism of Gammarus oceanicus and found an increase in standard metabolism following the Arrhenius equation over a temperature range of 5 ~ to 20~ (calculated from their Table 1). Routine rate differed substantially from the standard rate with regard to temperature sensitivity and first increased up to 15 ~ after which it again decreased. The authors related this to the different intensities of activity. In the present study, temperature affected the behavior of the three Calanus species significantly. Between 5 ~ and 10~ the time spent with HS decreased abruptly and copepods lay longer on the bottom, probably as a result of stress. Irregular swimming patterns in a copepod induced by a pollutant were observed by Cowles (1983). No clear relationship between temperature and any investigated index of activity could be detected, however, the time of active swimming as well as average swimming speed remained constant for C.finmarchicus, C. hyperboreus and Metrida longa. A clear trend towards a more energy consuming, faster swimming pattern such as jumps was also not observed. On the contrary, activity decreased almost linearly by a factor of 3 at temperatures between 0 ~ and 15 ~ in C. glacialis. Respiration rates increased with temperature, independent of activity. Thus, in Calanus glacialis, despite decreasing activity with increasing temperature, the "temperature characteristic"/, is similar to that of C finmarchicus, which showed a constant activity. The plateau in respiration rate at approximately 10 ~ found for C. glacialis and Metridia longa is not reflected in the activity. These observations lead to the conclusion that swimming activity did not contribute significantly to metabolic increase. The temperature-metabolism relationship observed therefore reflects mostly basal metabolism. The cost of swimming in small Crustacea has not yet been measured directly. Results obtained from models based on hydrodynamic theory suggest that swimming costs for small Crustacea range from negligible (Vlymen, 1970) up to 1.25 times the basal metabolic rate (Klyashtorin and Yarzhombek, 1973; Svetlichnyi etal., 1977). Recently, Morris etal. (1985) criticized these models. In their own model they analyzed the hydrodynamic forces which act on the copepod P{euromamma xiphias swimming at non-steady velocity. They found good agreement with empirical observations reported for larger crusta-
355 ceans (Ivlev, 1963; Halcrow and Boyd, 1967), in that swimming for copepods is relatively costly. However, the copepod species used in the present study performed the swimming mode modelled by Morris et al. (1985), namely the jump-and-rest mode, where the pereiopods produced the force, only to a small extent. In addition, the potential contribution of the antennules to propulsion, as suggested here, was not yet considered in their model. The main locomotor pattern performed by the Calanusspp. and Metridia longa is produced by rapid vibrations of the antennae, the mandibular palps, the mandibules and probably the maxillipeds (Lowndes, 1935; Gauld, 1966), which result in a smooth gliding. This eventually requires less energy than the intermittent swimming of cyclopids and P. xiphias with its short phases of high acceleration.
A cknowledgemenls. I gratefully appreciate the help of A. Herms in videoanalysis. P. Marschall provided computer programs and R. Bohrer assisted in respiration measurements. A. Spies made helpful comments on the manuscript. This is Alfred-Wegener-Institute for Polar and Marine Research Contribution No. 7. Literature cited
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Date of final manuscript acceptance: November 12, 1986. Communicated by O. Kinne, Oldendorf/Luhe
