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Limnol.
Ocennogr.,
24(e), 1979, 1081-1091
@ 1979, by the American
Society of Limnology
Effects of temperature
(Tunicata, Thaliacea):
vertical migration’
and Oceanography,
Inc.
on the swimming
Implications
for
of salps
C. R. Harbison
Woods IIole
Oceanographic
Institution,
Woods IIole,
Massachusetts
02543
R. B. Campenot
IIarvard
University
Medical
School, Boston,
Massachusetts
02115
Abstract
Salps swim by means of rhythmic contractions of the circular body muscles. In most species,
these contractions are regular. At constant temperature,
the pulsation rate is inversely related
to body length for hand-collected
animals. Such a relationship
is not seen with trawl-collected
salps. When temperature
is lowered experimentally,
marked differences
are seen in the response of individual
species. The pulsation rates of Pegeu confederutu,
CycZosuZpu poke,
and Salpa cylindricu
are greatly depressed and cease altogether at low temperatures
(response type I). For Pegea so&, CycZosuZpu pinnutu, Cyclosalpu affinis, and SuZpu maxima,
the pulsation rates are usually greatly depressed, but do not cease, even at extremely
low
temperatures
(response type II). The pulsation rates of Salpa fusiformis
and Salpa usperu
are largely insensitive
to changes in temperature
(response type III). Evidence
from net
sampling suggests a relationship
between these response types and vertical and horizontal
distribution
patterns. Salps showing response type I are found only in tropical and subtropical
surface waters; those showing response type II are more widely distributed
or are found in
temperate waters; and those showing response type III are vertical migrators. Thus, differences in the temperature
response provide clues as to the differing
modes of life available
to salps in the open sea.
Salps are transparent,
free-swimming
tunicates
found primarily
in the open
ocean, where they arc a widespread and
characteristic
fauna. They show considerable differences in size and morphology which may reflect different
adaptations to life in the open sea. The greatest
diversity of species is found in relatively
warm tropical and subtropical
waters or
in temperate
waters in the summer
(Thompson 1948; Yount 1958; Van Soest
1975), but several forms have been found
only in the Southern Ocean and Antarctic
waters (Thompson
1948; Foxton 1966;
Van Soest 1975). Of particular interest are
species in the genus Salpa, some of
which are primarily
tropical (e.g. Salpa
cylindrica),
while others occur only in
cold waters (e.g. Salpa thompsoni),
and
yet others are found over a wide range
(e.g. Salpa aspera).
Salps swim by rythmic contractions of
the circular
muscles of the body wall
(Fedele 1932). This method of swimming
sustained swimming
is very effective;
speeds of 550 me h-l have been measured
in the field (Madin 1974). The swimming and feeding processes are closely
linked-salps
must swim to feed (Madin
1974b). As they are thought to feed primarily
on phytoplankton,
salps have
been regarded as near-surface living animals, restricted
to the euphotic
zone.
There are, however, reports of salps at
great depths (Foxton
1966; Caldwell
1966) and an increasing body of evidence
that some species migrate over a considerable vertical range on a daily basis. Salpa thompsoni
has been reported
to
undergo a diel vertical migration (Mack* Contribution
4172 of the Woods IIolc Oceanointosh 1934; IIardy and Gunther 1935;
graphic Institution.
Research supported by the BiFoxton 1966). Foxton (1966) fLirther reological Oceanography
Section, National Science
ported that S. thompsoni
occurred
at
Foundation,
grant OCE 7521715 and OCE 7722511
and by the National Institutes of IIealth, Training
depths as great as 1,000 m. Franqueville
Grant~NS07009.
(1971) showed that Salpa fusiformis,
a
1081
1082
Harhison
and Campenot
closely related species, underwent a diel
vertical migration of some 500-800 m in
the temperate Mediterranean
Sea. Wiebe
et al. (1979) gave evidence for vertical
migration by yet another related form, S.
aspera; they found that the greatest biomass of this species by night was in the
upper 25 m, whereas by day, the greatest
biomass was in the 700-800-m sample.
Although they did not sample below 800
m, prior and subsequent visual observations from the DSRV Alvin indicated that
the bulk of the population
occurred at a
depth of between 800 and 1,200 m during
the day (Wiebe et al. 1979). We have also
found S. aspera and S. fusiformis
at the
surface during the night, but we have observed only scattered
and obviously
dying specimens of these species while
SCUBA diving in the upper waters during the day. Therefore, there is evidence
that at least three species of the genusS. fusiformis,
S. aspera, and S. thompsoni -undergo
extensive diel vertical migrations.
Vertical migrations
of this magnitude
are accompanied by temperature changes
of about 20°C and pressure changes of
about 100 atm. Pressure seems to have
complex effects on metabolic processes
(e.g. Hochachka 1975), but temperature
effects are usually unidirectional-an
increase in temperature causes an increase
in metabolic rate, unless some compensatory or buffering mechanism is present
(Prosser 1973). We here compare the effects of changing temperature on the frequency of the swimming
pulsations
of
migratory
and nonmigratory
species of
salps. There are pronounced
differences
in the effects of temperature on the pulsation rates of different salps, and these
differences may be related to whether a
species migrates vertically.
Differences
in the response to changing temperature
can also explain much about the geographic distribution
of several species.
We thank M. J, Greenberg for loaning
us the impedance converter, M. R. Reeve
for loaning us the vertically towed plankton net, and V. L. McAlister for preparing
the figures, L. P. Madin, V. L. McAlister,
N. R. Swanberg, W. E. Cross, and J. E.
Craddock
helped
these experiments.
us collect
salps
for
Materials and methods
Salps of both the solitary and aggregate
generations
were used in our experiments. Pegea confederata,
Pegea socia,
C yclosalpa
polae, C yclosalpa
pinna ta,
Cyclosalpa
affinis, Salpa maxima, and
Salpa cylindrica
were collected
with
hand-held jars while SCUBA diving during the day. The dives were made on RV
Oceanus Cruise 22 (tropical North Atlantic) and RV Atlantis II Cruise 101 (subtropical and temperate North Atlantic).
Station data for the dives are given by
Harbison et al. (1978) and Swanberg and
Harbison (in prep.). Since all our dives
were made during the day, salps that rnigrated into the upper waters at night
were collected with nets. The nets were
of two kinds: a horizontally
towed rectangular midwater trawl and a vertically
towed plankton net designed for the collection of soft-bodied organisms (Reeve
1977). Species collected with these nets
and used in experiments
were S. maxima, S. cylindrica,
S. fusiformis,
and S,
aspera. Except for a few hand-collected
specimens, salps were used in experiments immediately
after collection.
To measure the pulsation rate of a salp,
the animal was placed in a finger bowl
(loo-mm diam) containing seawater, and
a pair of fine wires, insulated except at
the tips, were sutured to the outside of
the tunic on opposite sides of the body.
The wires were fixed to the rim of the
finger bowl with wax, restraining the salp
from touching
the walls of the finger
bowl. The wires were flexible enough so
that they could be pulled toward one
another each time the salp contracted,
permitting
the rhythmic
pulses to be
timed by observing changes in electrical
resistance as the wires changed their relative positions. Electrical resistance was
monitored on Oceanus 22 with a Biocom
impedance convertor (model 2991), and
on Atlantis II 101 with a Harvard Apparatus impedance
pneumograph
(model
2191), and recorded with a Grass polygraph (model 5B). Ship-roll caused move-
Temperature
TEMPERATURE
1083
ejyects on salps
c°C)
Fig. 1. Temperature
profiles of four regions in
Atlautic Ocean where species were collected (data
from
Fuglister
1960). O-Equator
(OO”lci’S,
37”14’W);
H-northern
Sargasso Sea in summer
(34”04’S, 65”02’W);
~--slope
water in summer
North Atlantic
(38”54’N,
65”OO’W); l -eastern
(40”15’N, 33”13’W).
mcnt of the electrodes, but it was usually
of different form, amplitude, and period
from the movement caused by the contractions of the salp, and could be easily
distinguished.
In questionable
cases, it
was easy to check by counting the pulses
of the salp visually. The finger bowl was
placed in a larger container to which ice
or warm water was added to change the
temperature (Oceanus 22). To attain and
maintain lower temperatures,
a refrigeration unit was used on Atlantis ZZ 101.
The temperature of the seawater bathing
the salp was measured with a thermometer, and the pulsations of the salp served
to mix the water, so that the temperature
was probably uniform throughout the finger bowl provided that the salp continued to swim. Temperature was measured
with a thermistor (Yellow Springs Instr.
Co.) and recorded on the polygraph trace
on Atlantis ZZ 101.
Figure 1 shows typical summer tcmperature profiles for four regions where
we collected salps: Equatorial,
Sargasso
Sea, slope water off New England, and
eastern North Atlantic (Fuglister
1960).
The temperature profile of the equatorial
water is the same year-round and is almost identical
with that of the slope
water in summer. A salp migrating to a
I
10
I
I
20
30
TIME
I-I
40
50
60
(mln>
Fig. 2. Typical experimental
temperature
drop
(O), compared
with time-course
of temperature
changes that might he experienced
in first hour by
salps migrating vertically dowu from 100 m in equatorial regions (Fig. 1). Salps wo~lld experience most
rapid temperature
changes at thermocliue
(about
100-200 in). Rate of chauge cxperieuced
would depend on swimming
speed of salp. We calculated
time-course
of temperatures
that might be experienced by a vertically
migrating
salp for animals
moving vertically at 200 and 800 m *h-’ (see text for
justification
of these speeds). For slower animal,
this means a temperature
change
of about
-0.3”C*min-‘;
for faster animal, about -1.3%.
min-‘. Experimental
temperature
drop initially
is
ahout -0.7”C. min-‘, a compromise
between
extremes. To compare rates of change more easily, we
set all initial tcrnperaturcs
at 25°C.
depth of 1,000 m in one of these four major regions in the smnmer would undergo
a temperature change ranging from 14°C
(eastern North Atlantic) to 23°C (Equator). In our experimental
setup, we varied
temperature between 28” and 2.2”C.
We attempted to mimic the temperature changes that might be encountered
by vertically migrating salps at the Equator (Fig. 2). Madin (1974a) measured horizontal
swimming
speeds of several
species of salps and found that the slowest species swam about 200 111.h-l, the
fastest about three times as fast. When
observed in the laboratory, S. aspera appears more active than any of the species
timed by Madin, so it is reasonable to as-
1084
Harhison
I
and Campenot
I
0.6
BODY
LENGTH
Cmm)
I
1.0
I
I
I
I
1.4
1.6
2.2
2.6
WEIGHT
C mg
C 1
Fig. 3. Dependence
of swimming
rhythm at constant temperature
on size for Pegea confederata.
O-Solitaries;
O-aggregates.
a-Beats
per minute (bpm) at 25°C vs. length (y = -1.0X + 97, r = 0.89);
b-bpm
at 25°C vs. weight, as measured by carbon content (y = -0.018X + 77, T = 0.95). Differences
between the two generations are slightly reduced when compared on a weight basis.
sume that these salps may swim about
800 m. h-l. Although
we have no information about the speed at which salps
actually migrate, we used these two extremes of swimming
speed to calculate
the temperature
changes that would be
encountered by salps swimming straight
down, with no pauses, at the Equator
(Fig. 2). Our experimental
temperature
changes represent
a compromise
between the two extremes. Once the temperature reached its lowest point, it was
held there for variable lengths of time (up
to 2.5 h) and was then raised to room temperature (23’-28OC). Rewarming was usually faster than cooling. Pulsation rates
before cooling were compared with rates
after rewarming; if rates after rewarming
were significantly
lower, the salp was
considered to be damaged, and the data
were discarded.
Results
Of the nine species of salps we studied,
two (S. aspera and S. fusiformis)
have
been collected by us and coworkers on
only a few of the more than 750 dives we
have made in the upper waters of the
open ocean during the day. All of the other species are frequently
collected
by
daytime diving.
Several species show
non-overlapping
horizontal
ranges. Pegea confederata, C. polae, C. affinis, and
S. cylindrica
are found in the upper
waters of the tropical
and subtropical
western North Atlantic,
while P. socia
and C. pinnata are found mainly in the
temperate eastern North Atlantic. SaLpa
maxima is found in all parts of the North
Atlantic, however.
For some species pulsation rate is decreased markedly by cooling, others are
relatively
insensitive.
To compare these
results, we have calculated the ratio of
the pulsation rate at 20°C to the rate at
10°C. In accordance with the established
definition
(Prosser 1973) we term this ratio the Qlo value. Usually the shape of the
temperature
response curve was not exponential (see Fig. 5), so our use of the
term Qlo implies
no mechanism.
For
comparative purposes, we regard any Qla
value > 1.4 as high, and any value s 1.4
as low. Because the response to changing
temperature
is largely species-specific,
we will present our results by species.
Genus Pegea-The
physiological
responses of the two species of Pegea that
we studied differed greatly, in spite of
their close morphological
similarity
(Table 1). At constant temperature, the pulsation rate of P. confederata
was more
rapid than that of P. socia. For P. confederata, we observed an inverse relationship between body size and pulsation
rate (Fig. 3). The mean pulsation rate at
25°C for all specimens of P. confederata
was 48 bpm (beats per minute). This is
somewhat lower than the mean value reported by Madin (1974a), but the dis-
Temperature
1085
effects on salps
b
.,,
-\-‘
for a Pegea confederutu
solitary (length = 51 mm), showing constancy of swimming
Fig. 4. a-Record
rhythm of this species. Chart speed, 5 s. div- ‘; temperature,
23.5%; mean pulsation rate, 44 bpm. Most
salps we studied showed a constant pulsation rate such as this. b--Record
for a Salpa cylindricu
solitary
(length = 17 mm), showing irregular
swimming
rhythm characteristic
of this species. Chart speed, 5
se div-‘; temperature,
25.5%; mean pulsation rate, 96 bpm.
crepancy may be due to differences
in
the average size or differences
in the
temperature.
The swimming
rhythm of P. confederata was extremely
regular (Fig. 4a),
while that of P. socia consisted of bursts
of activity
and periods of quiescence.
Both species usually showed a marked
sensitivity
to changes in temperature
(Table 1). QIo values for P. confederata
-,
10
TEMP
CoC)
TEMP
Fig. 5. a-Effect
of temperature
on pulsation rate
at 23.5”C), showing typical type I response. Pulsation
on ordinate indicates temperature
at which pulsations
on pulsation rate of a S&pa maxima solitary (initial
response. c-Effect
of temperature
on pulsation rate
25”C), showing a typical type III response. All panels:
<oCI
TEMP
20
30
C°C)
of a Pegeu confederutu
solitary (initial rate, 44 bpm
rates expressed as percentages of initial rate. Arrow
resumed after warming. b-Effect
of temperature
rate, 47 bpm at 24”(Z), showing a typical type II
of a Salpa usperu solitary (initial rate, 60 bpm at
O-cooling
curve; O-warming
curve.
1086
Harbison
and Campenot
Table 1. Effects of temperature
on pulsation rate of salps in genus Pegeu. Pulsation rate at 25°C in
beats per minute (bpm). Qlo values are for interval of cooling between 20” and 10°C. In most cases,
temperature
response curve was linear, rather than exponential,
between these temperatures
(see Fig. 5),
so a least-squares regression line for data points was calculated, and values for pulsation rates at 10” and
20°C were used to determine Qlo. With P. confederutu,
salps stopped swimming at low temperatures.
Point at which salp stopped is given below, as well as temperature
at which it started up again. In some
cases, experimental
temperature was not low enough to cause salp to stop, so lowest temperature obtained
in a given experiment is also shown. Length of salp is given, since there is an inverse relationship
between
pulsation rate (bpm) and size (Fig. 3). Symbols for collection method on all tables: H-hand-collected;
Mmidwater trawl-collected;
V-collected
with the vertically
towed plankton net.
Length
(mm)
bpm at
25°C
QlO
stop
temp
CC)
Restart
yL;p
P. confederutu
30
33
50
47
51
60
60
62
67
51
38
43
46
35
31
30
2.75
5.17
3.67
3.24
2.00
29
38
45
60
72
63
59
45
2.78
4.35
-
23
24
24
26
28
29
37
40
41
35
2.02
1.97
1.58
2.10
1.32
* Restart
temperahlre
Collection
method
solitaries
s.0
ca. 5.0
7.5
19.0
8.3
P. confederutu
Lowest T
attained
(“C)
aggregates
10.0
6.0
-
P. sociu aggregates
-
19.0
*
13.0
20.0
12.0
20.5
14.5
-
-
12.5
5.0
14.0
5.0
7.5
11.0
19.0
6.0
II
II
II
H
II
H
H
l-1
10.0
6.0
16.0
16.0
H
H
H
H
2.2
7.7
6.0
3.2
3.5
H
H
H
H
H
not recorded.
were higher than for P. socia, but the
greatest difference
between
the two
species was that all P. confederata
ceased pulsating
at low experimental
temperatures
(< 10°C) whereas none of
the P. socia did. When specimens of P.
confederata
were rewarmed, there was
always a marked lag before pulsations resumed (Fig. 5a). This lag may be due to
an actual physiological
effect or to uneven warming.
Since the salp was not
swimming, the interior of the animal may
have been cooler than the water in the
finger bowl (see methods). Once the animal resumed
beating,
the resultant
warming curve was usually identical to
the cooling curve, showing complete reversibility
(Fig. 5a).
Genus Cyclosalpa-C
yclosalpa
polae
showed a temperature
response similar
to that of P. coqfederata: a high QlO, with
pulsations ceasing altogether at low temperatures (Table 2). In contrast, none of
the specimens of C. pinnata or C. affinis
stopped, although Qlo values were usually high. In one case, a very low Q10 was
observed with a C. affinis solitary. Both
C. polae and C. pinnata showed regular
swimming rhythms at constant temperature, but C. af$nis did not. For example,
for one specimen, pulsation rates at 25°C
for 40 successive 5-s intervals
ranged
from 30 to 63 bpm (mean rate = 53 bpm).
We used the highest rate sustained over
5 s for each temperature
in our calculations of Qro values. We reason that this
maximal rate shows the maximal capability at each temperature.
We could associate no change in gross behavior with
changes in pulsation
rate, as we were
able to do with S. aspera (see below).
Genus Salpa-At
constant temperature,
Temperature
1087
effects on salps
the swimming
rhythm of S. cylindrica
was irregular (Fig. 4b), and we saw no
differences in behavior to account for it.
Fpr example, for one specimen of S. cylid&a,
rates ranged from 61 to 110 bpm
(mean rate = 87 bpm). For this species,
as for others that had irregular swimming
rhythms, we have used the highest rate
sustained over a 5-s interval as representing the actual capability of the salp.
Use of the highest rate seemed preferable to averaging because salps have been
observed to pulsate at submaximal rates
during “escape responses” (Madin 1974a)
II--I
10
30
20
BODY
IL-40
LENGTH
I-_
50
80
8
TO
Cmml
Fig. 6. Dependence
of pulsation rate (bpm at
25°C) on body length for four species of S&m-S.
cylindrica,
S. maxima,
S. fusiformis,
and S. aspera. We used this relationship
to assess effects of
collection
method on experimental
results. l Hand-collected
S. cylindrica
and S. maxima;
Aindividuals
(S. usperu and S. fusiformis)
collected
with vertically
towed plankton net; O-individuals
(S. cylindrica,
S. maxima,
S. aspera, and S. fusiformis) collected
with midwater
trawl. Solid line is
least-squares
regression
line for data points obtained with hand-collected
individuals
(y = -0.98X
+ 110, r = 0.85); stippled area defines 95% conficlencc limits for these data points. All data points
Table 2. Effects
nation of quantities
of temperature
listed.
on pulsation
for individuals
collected
with vertically
towed
plankton
net lie within
or above stippled
area.
Least-squares regression line (y = - l.lX + 120, r =
0.78) through these data points does not differ significantly
from line through data points for handcollected individuals.
In contrast, most data points
for trawl survivors lie below 95% confidence limits.
Least-squares regression line (y = 0.079X + 50, r =
0.034) through these data points does not show relationship observed with animals collected by other
two methods. WC conclude that data obtained from
trawl-collected
animals are variably depressed.
rate of salps in genus Cyclosalpa.
stop
Lfxgth
(mm)
%Yt 0 1
70
21
Q*0
28.33
C. polae solitary
ca. 10.0
C. polae
28
28
30
32
14.34
3.53
60
64
72
38
37
31
3.22
2.17
2.77
50
52
23
23
1.68
1.75
36
50
21
45
1.05
1.62
28
36
60
33
2.93
2.01
Collection
method
6.0
II
23.5
ca . 14 .0
5.0
5.5
II
H
-
E
5:o
II
H
II
-
3.5
3.0
l1
II
-
-
5.0
10.0
H
II
aggregates
-
-
5.0
4.8
II
II
solitaries
-
C. pinnata
aggregates
-
C. affinis
C. uffznis
Lowest 7
attained
(“C)
1 gives expla-
18.0
aggregates
11.0
8.5
C. pinnata
,
Restart
temp
r-C)
temp
(“a
Table
solitaries
1088
Harbison
Table 3.
of quantities
Effects
listed.
of temperature
on pulsation
and Campenot
rate of species in genus Salpa. Table
stop
Length
(mm)
QlO
17
19
24
25
-
92
102
76
83
110
1.95
2.24
2.59
2.35
2.67
38
54
55
60
65
75
77
62
66
48
46
35
1.94
1.60
1.64
4.31
1.54
1.26
40
42
46
52
55
60
62
52
53
38
66
55
1.58
1.60
1.45
1.60
-
22
23
24
55
108
84
11
20
21
26
28
27
53
98
34
72
0.812
2.03
1.67
0.864
1.37
15
26
30
30
39
48
50
58
62
73
131
31
38
80
47
23
60
63
69
49
1.51
1.54
1.17
1.12
1.24
1.35
1.28
1.42
1.44
1.26
19
27
28
60
125
60*
64
53
Restart
S. maxima
Collection
method
‘g
t;Fy
S. cylindrica
5.5
6.0
4.5
6.0
5.0
1 gives explanation
solitaries
21.3
ca. 18.0
17.0
15.0
18.0
5.5
6.0
4.5
5.5
5.0
H
II
M
V
H
M
H
H
H
H
H
solitaries
-
-
10.0
-
1G
-
7.0
8.0
5.0
8.0
5.0
10.0
-
5.0
4.0
3.0
7.5
13.0
15.0
H
H
H
H
H
H
-
14.0
5.0
5.0
M
V
V
-
10.5
4.0
5.5
8.0
7.0
M
M
V
M
M
-
5.0
8.5
8.0
9.0
8.0
9.5
5.0
3.0
4.0
5.0
V
M
M
M
V
M
V
V
V
V
-
2.5
6.0
7.2
3.0
V
M
V
V
S. maxima
aggregates
S. fusiformis
solitaries
S. fusiformis
aggregates
S. asperu solitaries
* Rate at 25°C chosen
1.32
1.36
1.27
S. aspera aggregates
-
-
arbitrarily.
and while swimming
backward (see below).
Salpa maxima always showed a regular
rhythm at constant temperature.
If pul-
sation rate vs. length is plotted for all
hand-collected
S. cylindrica
and S. maxis found
ima, an inverse relationship
(Fig. 6). The swimming rhythms of S. ju-
Temperuture
effects on salps
siformis and S. asperu were always regular. However, reverse swimming
in S.
aspera
showed a slower pulsation
rate
than forward swimming.
For example,
one S. usperu had a forward rate of 63
bpm at 25”C, a reverse rate of 51 bpm.
We have presented only the forward rates
in tables and figures.
The temperature responses of the four
species of Sulpu differed markedly (Table 3). Salpa cylindricu
gave a response
similar to those of P. confederutu and C.
po2ue. The temperature
response of S.
muximu usually resembled that of P. sociu, C. pinnutu, and C. uf$nis (Fig. 51~).
However, the pulsation rates for S. fusi*formis and S. usperu were affected very
little by changing temperatures.
We could not detect an unequivocal
response to changes in light intensity
ranging from total darkness to full daylight illumination.
In seven experiments
with S. usperu, we found a response to
changes in light intensity in only two. In
one, the amplitude, but not the frequency, decreased at high light intensities.
In
the other, the frequency decreased at low
light levels. Thus, although S. usperu can
detect low levels of light, the nature of
the responses is not predictable.
Our observations
contrast with the results of
Mackie and Bone (1977) for S. fusiformis; they saw a decrease in pulsation rate
at high light intensities.
Effects of net truumu on experimental
results-Collection
by hand should be
the best method. All of the animals collected with the vertically
towed net also
appeared to bc in good condition, so we
judged that this method caused little injury. In contrast, most salps collected
with the horizontally
towed midwater
trawl were dead or grossly damaged. A
small proportion appeared to be in good
condition,
and only these were used in
experiments.
To evaluate the collection methods, we
plotted the prllsation
rate at 25”~ as a
function of body length for hand-collectec3 S. muximu and S. cylindricu
(Fig. 6).
An inverse relationship
is observed, as
with P. confederutu
(Fig. 3). This relationship probably holds for all’ salps. We
1089
calculated a least-squares regression line
and 95% confidence belts for these data
points (Fig. 6).Because all of the data
points for animals collected by vertically
towed nets lie within or above these belts
(Fig. 6), we conclude that the vertically
towed net causes as little injury as hand
collection.
In contrast, most (8 of 13) of
the data points for the trawl survivors (S.
maxima, S. cylindricu,
S. usperu, S. fus<formis) lie below the lower 95% confidence limit (Fig. 6). We conclude that, in
spite of their appearance,
even the
healthy-looking
trawl survivors
were
damaged, resulting in a variable depression of the pulsation rates. Absolute rate
measurements
on other organisms collected with horizontally
towed nets are
likely to be similarly affected.
Although collection with the midwater
trawl caused a depression in the absolute
rates, there was little effect on the Qlo
values. There appears to be no relationship between collection method and the
magnitude of the temperature effect (Table 3). Although
relative rate mcasurements may not be affected, we recommend a skeptical attitude toward absolute
rate measurements
made on net-collected specimens.
Discussion
The species we studied can be divided
into three categories, based on their responses to changing temperature.
The
pulsation rates of those in the first category (response type I) are markedly affected by changing temperature (Qlo values >1.4),
and these animals
stop
pulsating
at low temperatures.
Pegeu
confederutu,
C. polue, and S. cylhdricu
all show the type I response. The second
category (response type II) is characterized by a marked sensitivity
to changing
temperature
(Qlo values >1.4), but the
salps do not stop pulsating. Most P. sociu,
C. pinnutu,
C. affinis, and S. muximu
show the type II response. The third category (response type III) is characterized
by very little sensitivity to changing temperature (Q,,, values ~1.4). Most S. fusiformis and S. usperu show the type III
response. Although
the correspondence
Hurbison
und Cumpenot
RESPONSE
TYPE
S. fusiformis
S. aspera
I
I
I
I
I
I
2
4
6
2
4
6
I
2
4
6
Fig. 7. Histogram summarizing
our classification
of species on basis of response types for all salps
of solitary individuals;
exposed to experimental
temperatures
of 10°C or lower. Open bars-number
hatched bars-number
of aggregate individuals.
Three species (P. con&Aeruta,
C. poke, and S. cy2inckica)
always showed the type I response, accounting for 14 of the 15 times (93%) we observed it. Two species
(S. fusi~ornzis and S. usperu) accomlted for 86% of the times we observed the type III response (see text
for definition
of response types).
between response type and species is not
perfect (Fig. 7), we conclude that insensitivity of pulsation rate to experimental
cooling is associated with absence from
surface waters during daylight. Salps are
found primarily
in the open sea-an environment characterized by great thermal
stability (Fuglister
1960). Therefore, one
would expect to find physiological
adaptations to rapidly changing temperature
only in species that migrate vertically.
Indeed, this should be true of all other
oceanic organisms as well. Our experimental results support the present sampling evidence that S. fusiformis
and S.
usperu
do migrate vertically
(Franqueville 1971; Wiebe et al. 1979).
We do not know whether the effects of
temperature
on pulsation
rate mirror
comparable effects on metabolism. Mackie and Bone (1977) confirmed the finding
of Fedele (1932) that there is a neural
pacemaker for the swimming
rhythm in
the brain. The effects we see may be acting only on the pacemaker or may reflect
a more general effect on metabolism.
Our results are also in accord with
present
zoogeographic
information.
Species limited to tropical and subtropical waters all show the type I response.
P. confederutu
has not
For example,
been found in waters colder than 16°C
(1Madin and Harbison 1978), and S. cylindricu has not been found in waters colder
than 17°C (Van Soest 1975). In contrast,
the species showing response type III
are either widely distributed
(S. muximu,
S. usperu, S. fusiformis)
or are found ex-
Temperuture
effects on sulps
elusively
in temperate waters (P. sociu,
C. pinnutu) (Madin and Harbison 1978;
Harbison and Madin unpubl.).
Zoogeographic information
on C. uffinis (Van
Soest 1975; Harbison
and Madin unpubl,) is not in accord with its response
type classification;
its distribution
is similar to that of the type I species. However, it might be predicted that it, as well
as other response type II species, could
range to greater depths. Present zoogeographic information
on salps is very liinited, and fLirther data, incorporating
the
most recent taxonomic
revisions,
are
needed before our classification
of physiological response types can be adequately tested.
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Submitted:
Accepted:
26 June 1978
14 May 1979