ARCHIVES
FISHERIES RESEARCH BOARD OF CANADA
Translation Series No. 973
On the efficiency of utilization of energy in
pelagic ecosystems of the Black Sea
By T. S. Petipa
Institute of Biology of the Southern Seas
of the Academy of Sciences of the Ukrainian SSR
Original title: Ob effektivnosti ispol'zovaniya energii
pelagicheskikh ekosistemakh Chernogo Morya.
From: Struktura i dinamika vodnykh soobshchestv i populyatsii,
pp. 44-64. 1967. Respublikanskii Mezhvedomstvennyi
Sbornik, Seriya "Biologiya Morya". Akademiya Nauk
Ukrainskoi SSR. Published by "Naukova Dumka", Kiev.
Preliminary translation by W. E. Ricker
Fisheries Research Board of Canada
Biological Station, Nanaimo, B. C.
1967
This is a preliminary translation prepared
for the use of the Fisheries Research Board of
Canada. It is not a definitive English version
of the article, and it has not been checked or
approved by the author.
On the efficiency of utilization of energy in
pelagic ecosystems of the Black Sea
By T.S. Petipa
One of the most recent trends in hydrobiology is the
study of ecological systems, or ecosystems for short. An
ecological system comprises a biotope with its inhabitants
(Odum, 1959). The study of ecological systems makes possible
predictions concerning large-scale biological phenomena in a body
of water.
z
A stream of matter and energy courses through an ecosystem.
The solar energy used by phytoplankton is transferred from the
first, autotrophic, level to the next, heterotrophic, level when
the algae are eaten by animals. At each trophic level part of the
energy is released in the form of undigested remains, and part is
assimilated. The assimilated energy is partially used for metabolism of the organisms concerned and consequently is lost to the
productive process. Another part of the assimilated energy is
used for growth of the organisms, is incorporated into them, and
is then handed on to the following level.
With these basic paths of energy distribution of food
chains in mind, we may consider that one of the main problems in
studying ecosystems is the problem of the efficiency of utilization
of energy by different ecological systems. The following question
is of great theoretical importance: do ecosystems differ among
themselves in their efficiency of utilization of energy? If they
differ, these additional questions arise: what are the different
types of ecosystem that may be distinguished on this basis? and
what do the differences between ecosystem types consist in?
;
It will be possible to answer these questions only by
studying the biology and interactions (especially food interactions)
•
-2
of actual species that occur in massive numbers, with a concurrent
[page 45 1 analysis of their distribution in time and in space.
These are the objectives which we have set ourselves in studying
the ecosystems of the Black Sea.
In the pelagic region of the Black Sea there is a welldeveloped two-layered distribution of complexes of organisms.
The upper, epiplanktonic, complex inhabits the surface strata
above the thermocline, while the deeper, bathyplanktonic,
complex occurs from below the thermocline down to the limits
of convective mixing in winter, sometimes as far as the hydrogen
sulphide zone. The first complex occupies a thin layer, from
5 to 20 m deep. This layer is well-lighted, it becomes warmed
to a higher temperature, during the greater part of the year it
has a higher rate of production of phytoplankton, and it is inhabited by abundant epiplanktonic crustaceans -- copepods,
cladocerans and several other organisms, which almost never
leave this layer. The second -- bathyplanktonic -- complex
occupies a considerably more extensive region, from 5-20 to
60-150 m. This is a cold layer, and the temperature and quantity
of food in it decreases with depth.
In this layer Calanus and
Pseudocalanus predominate; they migrate throughout the whole
layer, and also sometimes ascend to the surface.
These two complexes of organisms, and two water layers,
are the two ecosystems in which the efficiency of utilization
of energy by populations of the predominant plankton species
have been investigated. Inasmuch as the two species selected
are each typical of their ecosystems in the Black Sea, and the
behaviour of the other species in each ecosystem is similar,
we may assume with considerable confidence that a picture for
all the species of each ecosystem considered as a whole will
be close to the picture which we obtain for these selected
species, in respect to utilization of energy.
-3
A two-layered distribution of complexes of organisms
in pelagic waters is of very wide occurrence. Hence other
ecosystems of baroclinic seas, inhabited by other ecological
types, may also be studied by the method suggested below.
In the present paper some preliminary results of our
studies of these ecosystems are presented based on data obtained at a station that was occupied for many days in June
of 1959 in the western qalistaza of the Black Sea. The
boundary between the systems at that time lay at a depth of
12 m. The basic quantitative information on each system was
obtained from the data of two or five 24-hour stations.
Methods
In order to study the efficiency of utilization of
energy by these ecosystems an anatomical and physiological
description was made of the principal copepods in the two
complexes -- Acartia clausi Giesbr. and Calanus helqolandicus
[page 46] In addition their distribution, in terms
(Claus).
of numbers and biomass, was measured throughout the whole water
column and over the course of the 24-hour day. Along with this
the daily change in biomass of each of the phytoplankters and
zooplankters in the individual strata was determined; as was
the rate of cell division of the phytoplankton in glass vessels
suspended in the sea, as well as in laboratory cultures at
temperatures and illuminations corresponding to those of
different depths (data of L.A. Lanskaya).
Methods of locomotion and of capturing food were studied
over the whole life cycle of both species, by means of a functional investigation of their external structure, feeding
rhythm, composition of their food, selective capacity and
the influence of the size and movements of food objects on
their availability as food, daily rations, duration and degree
4
of digestion of the food, increase in size, quantity of oxygen
consumed, expenditure of organic matter and energy in metabolism,
and satisfaction of the food requirements of these crustaceans
in the sea. The problems just enumerated were attacked by a
combination of experimental and field methods. From the data
obtained an energy balance was computed for both species and
the different stages of development and life forms were compared (Humboldt, 1806; Akimov, 1954; Beklemishev, 1964;
Petipa, 1967).
Methods and results of these investigations have been
set forth in special works (Petipa, 1957, 1959, 1959a, 1960,
1966, 1966a). In a majority of cases the experimental methods
used have provided reliable and consistent results. However,
in studying Calanus the usual laboratory methods were frequently
unsuitable because in the laboratory it was impossible to provide a migration path for these crustaceans that was 50-100m
high. It was necessary to use a new method for determining
the expenditure of energy in metabolism of Calanus at sea,
the rations that meet these requirements, and their consumption
of food objects in the sea (Petipa, 1964, 1964a, 1965, 1966b).
This method consists in a determination for these crustaceans
of the quantity of freely impregnated fat [svobodno vkraplennyi
zhir] that is used for metabolism in the course of 24 hours,
particularly during movement, or is stored up during the
feeding period. The stores of fat in this copepod serve
as its main source of energy expended in metabolism. Determination of the ration among Calanus has led to an evaluation
of the quantity of food [consumed], from which comes the fat
stored in layers along the digestive tract, and [subsequently]
used up, during the course of a 24-hour day.
From Fig. 1 it is evident that among Calanus of the
older stages the daily oxygen requirement and the energy expenditure for metabolism in the sea was 31-35 times higher
-5
than the energy requirements of animals of these same stages
under laboratory conditions, that is, in the absence of migration.
At the same time, among the non-migratory younger groups
identical figures are obtained by both methods in the laboratory
and at sea.
[page 47] The following parameters have been used to
evaluate quantitatively the efficiency of production and
utilization of energy by the communities of an ecosystem and
their component populations. All quantities are expressed
in the same units (gram calories) and are referred to a single
unit of time (the 24-hour day).
1.
K 1 and K 2 -- coefficients of utilization of energy for
growth of the first and second orders (Ivlev, 1939,
1939a): the ratio of energy of growth of the organism
to the total energy consumed (for K 1 ), or to only the
energy assimilated (for K 2 ). In this paper both
coefficients are computed for individual growth
stages of the species studied, on the basis of the
mean daily increment in biomass, metabolism, and
the consumption [potreblenie] and assimilation
[usvoenie] of food. 1
L. Slobodkin (Macfadyen 1965)
has proposed a related index of efficiency of growth
of animals: the ratio of energy contained in the
animal's tissues to the total energy that it contained at birth and had used subsequently in the
growth process.
irLAlthough
Petipa does not say so explicitly,
that assimilation -- usvoenie or assimilyatsiya -include nitrogenous or other wastes excreted after
absorbed through the gut; in other words it is the
logically useful energy" of Ivlev and Winberg.]
it appears
does not
first being
"physio-
6
[Page 47j
0,013
0,01
0,005
2
goo
0,25
0,5
3
475
fig. 1 - Comparison of the energy metabolism of Calanus
helgolandicus under natural and laboratory conditions.
1 - consumption of oxygen by these crustaceans in the
sea (based on fat consumed);
2 - consumption of oxygen under laboratory conditions
(according to Marshall and Orr, 1958);
3 - consumption of oxygen under laboratory conditions
as calculated from Winberg's (1956) formula;
4 - consumption of oxygen under laboratory conditions
computed from fat consumption.
-7
2.
-- efficiency of production [produtsirovanie] of biomass:
the ratio of the energy of growth of a population, or
of the sum total of populations of one trophic level
[P], to the total energy required by the given
population or level for the elaboration [obrazovanie]
of this matter [veshchestvo], that is, to the total
energy assimilated [U].
Two of the coefficients just described -- K 2
and P/U -- may be regarded as performance coefficients
[koeffitsienty poleznogo deistviya] for the organism,
population or trophic level under consideration. 2
3.
-- the relative rate of production of biomass: the ratio
of increment of the population [P] to the average
biomass of the population present during the period
in question [8].
[page 48]
4.
2
--
5.
E
--
the relative rate of energy consumption [skorost'
energicheskikh trat] by a population: the ratio
of energy expended in metabolism by the whole
population [Q] to the mean biomass of the population [8].
relative rate of uptake [pritok] of energy by the
population: the ratio of the quantity of energy
asimilated by a given population [U] to the mean
biomass of that population [B].
2
[In other words K 2 and P/U are essentially the same
parameter, the former used
for individual organisms and the
latter for groups. Similarly K, would be analogous to P/R.]
8
6.
7.
8.
-- relative rate of consumption [potreblenie] of energy
by a population: the ratio of all energy consumed
(the food eaten) by the population [R] to the mean
biomass of the population [B].
R'
the efficiency of extraction [izyatie], or
B'Ph
Pf
consumption [vyedanie], of energy (of vegetable
food) by a population: the ratio of the energy
in the food eaten by a given population [R'] to
the energy of all such foods in the sea that are
either in existence [B'P h ] or are created [P f ]
[during the time-interval under consideration].
This coefficient is important in ecological
contexts, for it indicates the degree to which
a population makes use of its food supply.
[This is Ivlev's (static) ecotrophic coefficient. - W.E.R.]
p
B'Ph
-- the relative rate of potential production of
biomass of phytoplankton:
the ratio of the daily
potential production of phytoplankton [P ] to the
original minimum biomass of phytoplankton present
during the day -- specifically during the early
morning hours [Bhh ].
B'P h is the biomass of phytoplankton, including
Noctiluca.
P
the daily potential production,of phytoplankton,
P,
2 t /V
is equal to B 1 - Bo , where B 1 = B,
(t - 1 24-hour day).
= the time between fissions of the algae
[in days].
B 0 = the original minimal biomass present.
This coefficient shows the potential productive capacity of
the phytoplankton under the existing external conditions,
particularly of illumination, temPerature, content of biogenic elements and prevailing abundance. Since in this
situation we have in mind only the increase in mass of matter
[prirost massy veshchestva], the potential production under
consideration is the "net" [chistaya] production of Clarke
(1946) or the "effective" [effektivnaya] production of
Kalle (1948) and Elster (1954).
9.
Pf
B'Ph -- the relative rate of actual [fakticheskii] or
real [real'nyi] production [produtsirovanie] of
biomass of phytoplankton: the ratio of production
[produktsiya] actually achieved (mass of substance)
by phytoplankton in the sea, under the existing
external conditions and [rate of] elimination [P f ] '
to the original minimal biomass of phytoplankton
present [11q)1,1 ].
[page 48] This coefficient is especially important in ecological contexts, since it shows how elimination -- mainly
consumption -- affects the magnitude of phytoplankton production. In situations where all the phytoplankton production
is consumed, its actual production may be estimated from the
mass of phytoplankton eaten.
In addition to the coefficients just mentioned, two
more indices were computed which indicate the relationship
between primary production and the biomass of the whole
community:
10.
—2
Bs
--
the ratio of potential production of phytoplankton
[P ] to the total biomass of the community [B e ].
IP
- 10 -
P
11. --f -- the ratio of the actual production of phytoplankton [P f ] to the total biomass of the
B5
community [B s ].
Results
•
Before we turn to a consideration of the data on
efficiency of utilization of energy by populations and
communities, it is necessary to give a brief description of
the different life forms of Acartia and Calanus, which characterize the epiplanktonic and bathyplanktonic communities
respectively.
During their life cycles Acartia and Calanus pass
through 12 stages of development, separated by molts. Over
the length of the period from the egg to sexual maturity five
life forms may be distinguished in both species (Petipa, 1967).
The first period of development of these copepods, or
the first life form (the egg stage), consists of the embryonic
development which occurs in the water. In the two species this
life form proceeds identically.
The nauplial and copepodite periods each include two
life forms.
The first nauplial life form in both species (Stages I-II)
is characterized by absence of feeding and by an identical
type of movement produced by beating with the second antennae
(small jumps).
The second nauplial life form begins after the completion of the development of the first life form at the
expense of the embryonic yolk, and the transformation to
nauplial stage III. The entomostracans then begin to feed
on vegetable foods, and they move by several methods -- by
- 11 -
occasional sharp jumps, by frequent small jumps, and by smooth
gliding. All these types of movements among the nauplii are
as yet poorly developed because they are associated fundamentally with beating by the oral appendages which at this time
are not well developed.
[pages
50-51 - Table 1]
52] The principal organ for movements of the type of
sudden large leaps, the abdomen, is completely absent in
Acartia nauplii while in Calanus nauplii it is replaced by
the constricted posterior part of the body (Fig. 2 and 3).
As a result of the poor development of apparatuses for movement, filtering and grasping, search for and capture of food
is difficult for nauplii, and they cannot procure themselves
a large enough quantity of food for rapid growth. As a result,
the rate of growth of nauplii is usually less than that of
copepodites.
[page
Thus nauplii expend much energy in movement and grow
rather slowly. The coefficient of utilization of energy for
growth is low in both species:
for Acartia K 2 = 17%, and
for Calanus K 2 = 37% (Table 1). The larger growth coefficient
among Calanus nauplii results from their smaller expenditure
of energy for metabolism associated with a better means of
locomotion using the narrowed posterior part of the body.
The rate of movement of Acartia nauplii, by means of small
jerks, is equal to 0.4-0.8 cm/sec, while for Calanus nauplii
it is 1.5-2.4 cm/sec.
53] With the transformation to the first
copepodite life form the body becomes separated na taomy:
the cephalothorax and the abdomen. The masticatory apparatus
continues to be perfected (although in its-general features
it was already formed), and also the means for capturing food,
[page
Table 1. Relation between increase in weight, expenditure for metabolism and food requirements for the epiplanktonic
Acartia clausi and the bathyplanktonic Calanus helgolandicus (in calories and ,as percentage of the average
energy content of the food during each period of developme4
Male
Femalel
Unit
Second copepoàit
Arartio clime
Copepodites
iv
I ut
Lv
life form
It
First copepodite life form
.
Mean daily increment
Ca l crie s
x.1 6-11
r
auplii
Second
nauplial
life form
3,3
1,2
16,50
8,3
16,81
13,7
17,26
24,3
5,81
18,2
3,76
21,3
1,27
20,3
eggs
Metabolism per day
Kanopm.10-4 128,00
53,1
143,10
51,6
100,26
49,8
67,10
55,0
43,03
60,6
22,55
70,2
13,93
79,1
5,99
98,2
Daily ration
Kanopila•10-4 161,00
es
66,4
180,85
65,0
145.95
72,6
104,89
85,9
75,36
106,1
35.45
110,4
22,11
125,5
9.07
148,1
Assimilated portion
ot the ration
}Canopus • 10-4 128,00
146,40
52,8
116,76
58,1
83,91
MJ
60,29
84.9
28,36
88,4
17,69
100,4
7,26
118,5
2,0
14
20
29
21
21
17
1,8
11
16
23
16
17
14
,
K2
53,1
increment X 100
asamilated portion
of the ration
increment
x 100
_
K2_
tation
1
Calanus helgolandiais
Mean daily increment
Calories %
0,043
3,2
0.066
5,9
0,135
21,5
0,054
21,7
0,022
22,5
0,008
21,0
0,0 01
6,3
Metabolism per day
Kanopiin
1,408
102,6
1,639
121,4
1,110
98,3
0,4515
71,9
0,1221
48,8
0,0234
29,0
0,006-18
17.1
0.00167
10,4
Daily ration
Knoplin
1,564
114,0
1,869
138,4
1,306
115,6
0,6510
103,2
0,1950
78,0
0,0560
57,1
0.01600
49- , 2
0,00296
18,5
Ka.nopisn
1,408
102,6
1,682
124,6
1,176
101,2
0,5865
93,4
0,1761
70,5
0,0504
51.5
0,014-18
33,0
0,002a
163
ssimilated portion
of the ration
increment x 100
K ' assimilated portion
of the ration
K,-increment x 100
ration
es
96
6
23
31
43
55
37
96
5
21
98
39
50
34
4*
51
- 13 -
[Page 52]
CM
D
Fig. 2 - Changes during development in the size relationships
between the parts of the body, its cross-section, and the
amplitude of the strokes of the abdomen, in Acartia clausi.
1 - nauplius, 2 - copepodite I, 3 - copepodite III,
4 - female, 5 - male, C - length of the greatest width
of the body, D - amplitude of the strokes of the abdomen,
Cph - cross-section of the cephalothorax in the region
of its greatest width,
Abd - cross-section of the abdomen at its articulation
with the cephalothorax.
- 14 -
[Page 53]
-e-
-e-
-ED
e
_M21
Fig. 3 - Changes during development in the size relationships
between the parts of the body, its cross-section, and the
amplitude of the strokes of the abdomen, in Calanus helgolandicus.
as in Fig. 2.
Explantio
"4-15 and for locomotion. The small copepodites are as yet not
capable of moving any considerable distance because of the
imperfect development of the abdomen. The latter is less
moveable, is considerably broader relative to the greatest
width of the body (cephalothorax), and is somewhat shorter
relative to the total length, than among older copepodites
(Table 2, Fig. 2; 3). These tiny crustaceans live in a
single stratum, that is rich in food. They feed intensively
throughout all or almost all of the 24-hour day, and they grow
rapidly. Among both species there is a high mean daily increment of growth for a short period of time. Their requirements of energy for metabolism are not great (Table 1).
Comparison of,these rapidly-growing stages of Acartia
and Calanus shows that Acartia grows more slowly than Calanus.
This results from the fact that Acartia expends a larger
portion of its energy in movement, since on the one hand its
swimming is less effective, and on the other hand it continues
throughout the whole 24-hour day. During the same period the
copepodite stages of Calanus, which are also growing intensively, remain in a rather inactive condition for part of the
day; [page 55 1 thus they economize their energy, and what is
saved can be used for growth.
The greatest percentage of physiologically useful
energy used for growth is observed in Calanus, especially
in its copepodite stages (K 2 - 43-55%). In Acartia this
growth coefficient of the second order is only half as large
as in Calanus (K 2 = 21-29%) (Table 1). The same relationship is observed between the coefficients of utilization for
growth of the total energy consumed, that is ) between the
growth coefficients of the first order (K ). In Acartia K
1
1
is only half as great as in Calanus, just as is true of K 2
(Table 1). Thus the rapidly-growing Calanus utilizes its
food more efficiently.
- 16 -
[Page 54]
Table 2 - Size of the parts of the body (in mm) and their ratios (as percentage)
among Black Sea Calanus heloolandicus and Acartia clausi (after Petipa t 1957).
Size anci ra±t0
Males remalee
C o loerOd 1 . 1- a5
V
I
Iv I III I
e mbe pod;beri
Males
II
V
C. helgolandlcus
Ln
1L
of
gephaloKor.1*
cf oehhalotho,-ax
Length of abdomen
vs/I'crtt.-■ of abdomen
Total body I enek
04- e.ephalo±lItit_41
Lenit-i, of
2,222
0,700
0,581
0,157
2,803
1,689
0,515
0,448
0,130
2,137
1,290
0,382
0,328
0,104
1,568
0,931
0,270
0,253
0,090
1,184
0,708
0,222
0,194
0,081
0,902
0,855
0,300
0,277
0,065
1,132
0,905
0,306
0,295
0,070
1,200
0,625
0,203
0,192
0,051
0,817
A. claus1
0,564 0,439
0,201 0,154
0,168 0,114
0,04 7 0,038
0,732 0,553
11
0,319
0,102
0,090
0,031
0,409
0,253
0,100
0,073
0,029
0,326
25,3
25,0
24,1
24,3
23,0
24,6 26,6
34,3*
25,5
29,8
27,5
27,8
25,0
30,7*
23,0
21,1
20,7
21,0
20,9
21,4
21,5
24,5
24,6
23,5
22,9
20,6
22,0
22,4
abdomen
eephalofhorax
29,9
26,7
26,2
26,4
26,5
27,1
27,1
32,3
32,5
30,7
29,8
26,0
28,2
28,8
o4. abc(c)rnen
22,1
23,4
22,4
25,2
27,2
33,4
36,5
21,7
22,8
25,1
23,4
24,7
30,4
29,0
1,13
1■1•111
■•■••■
1,00
■■•■■•
o1
bIcto rne
o-ç 0.11
Lo-n5th of
vs/i .4141
2,604
0,837
0,697
0,196
3,301
I III'
25,1
\Wet/
Len j
2,428
0,791
0,726
0,175
3,154
nr
Wi'd+h cf dephalothoraX
Wide, of eepho1o4iorax
Thiek.nes o4 ce.ephalothorax
or base,
ThieKne,s5 of ba.5
O?
a6Jornen
of abdomen
1,10
1,13
1,32
1,00
1,00
1,33
Immediately after transformation from the nauplius.
■•••
•■■•••
MUM,
1,33
1,33
-17 -
After transforming to the second copepodite life form
growth slows down abruptly in both species, while the abdomen
and the oral appendages with their corresponding armament
becbme fully developed. These entomostracans are now able
to perform vertical migrations, and can also capture both
small and large foods by several methods. For the development
of,the gonads, production of eggs and performance of their
daily vertical migrations the entomostracans require either
a large quantity of plant food (Calanus) or a relatively
smaller quantity of mixed food -- plant and animal (Acartia).
Among migrating entomostracans of both species there has been
observed a more or less pronounced preponderance of night
feeding over day feeding. Among the good migrators (Calanus)
day feeding may even be absent. It is during the second
copepodite life form that the greatest differences between
the two species occur, these being associated with increased
differences in body structure and behaviour. For example,
the older stages of Calanus, when they have reached a large
size and have a more streamlined body form, perform daily
vertical migrations of great amplitude (50-90 m) and speed
(12-15 cm/sec). The older stages of Acartia are considerably
smaller and have a less streamlined body form, particularly
in respect to the square front and the long spinules along
the whole length of the antennules. In consequence Acartia
migrates for only a short distance (10-15 m) and at a slow
rate of speed (2.5 cm/sec).
To perform these large migrations the older stages of
Calanus use a special source of energy in the form of periodically accumulated fat. A considerable quantity of fat is used
up every day and for its daily replacement a large' quantity of
food is required. Thanks to a special and complete development of the oral appendages, and to their possessing several
means of capturing food, Calanus of the older copepodite
•
-
18 -
stages are adapted in the best . possible manner to capturing
phytoplankton organisms of different sizes and shapes.
[page 56] Calanus can obtain this food in sufficient quantity
only in the upper strata of water, during their night-time
ascent. During daylight hours the older stages of Calanus
are found at lower levels, and in a passive condition. The
older stages of Acartia,by contrast, practically do not
accumulate fat, since they expend much energy in their
continuous around-the-clock movements in a thin stratum of
water. They occupy an intermediate position between plant
eaters and animal eaters, and therefore do not exhibit very
complete adaptations for either the one type of food or the
other. To provide themselves with the quantity of food they
need, the older copepodite stages of Acartia, just like the
younger ones, must feed around the clock.
In connection with these changes in the behaviour of
Calanus with age, along with the strong intensification of
migration there is an increase in their daily energy requirement for total metabolism, per unit body weight; in Acartia,
on the other hand, there is a decrease, which is associated
with the rather small increase.in amplitude and speed of
migration as this entomostracan increases in size. Although
during its migrations Calanus moves at speeds 5-10 (sometimes
even 20) times greater than Acartia, nevertheless the daily
energy requirement for metabolism, as a percentage of body
weight, among migrating Calanus of the older stages (107%),
is only twice as large as the corresponding value for the
same stages of Acartia (52%) (see Table 1).
Thus comparison of the life forms of the epiplanktonic
Acartia and the bathyplanktonic Calanus throughout their life
cycles has shown that similarity between the two species is
to be found only in their development; while differences
- 19 associated with the structure of the body and the mode of
life of each species are exhibited in the preponderance of
one or another method of locomotion, in the composition of
their food, in the rhythm of feeding, in the size of their
rations, in the character and speed of their migrations, and
in the associated energy requirements for growth and for
metabolism. These differences are especially clearly exhibited in the final stages of the nauplial and copepodite
periods of development, that is, in the second nauplial and
second copepodite life forms (see Table 1).
It is interesting to observe that the characteristics
of the development of adaptations to rapid swimming in the
ontogenesis of fish and of copepods are similar in their
general features. According to the data of V.V. Shuleikin
(1953) and Yu.G. Aleev (1963), among the less rapidly moving
fishes (which includes the young of all fishes), that swim
with a wavelike type of body motions [izgibaniya], the locomotory function is distributed more or less evenly along the
whole axis of the body in a longitudinal direction. In this
case the body commonly has an elongate, eel-like form, it is
more or less uniform in depth along its whole length, and it
is uniformly flexible along almost its whole length. If the
depth of the body varies, there must be compression of the
body in the plane of bending [where the depth is greater].
[page 57] With the change to rapid swimming the
function of locomotion is accomplished mainly by the hind
half of the body, as a result of which the body of the fish
assumes a scombroid form, it becomes shorter, compact, plump,
smooth and well streamlined. The tail fin is joined to the
body by a taperqd stiff caudal peduncle, all of which makes
possible great frequency of alternation of movements of the
caudal portion of the body, and abrupt changes in the direction of these—movements.
-2 0 -
The movement of a copepod by means of frequent strokes
of the abdomen, with its fan of furcal spinules in the horizontal plane, is to some degree reminiscent of the good swimmers -fishes and whales. Hence we may conclude that since the change
in body form of a copepod during ontogenesis proceeds in the
same direction as among fishes -- from the eel-like to the
scombroid type -- then this involves the acquisition of a
more finished form, adapted to relatively rapid swimming.
This conclusion is confirmed by actual observations on the
speed and nature of the movements of Acartia and Calanus of
different ages, and on the agreement between the external
structure of these entomostracans and their swimming ability
(see Fig. 2 and 3 above) (Aleev, 1963). Although copepods
have a more rigid construction of the parts of the body than
fishes do, nevertheless some bending of the body is possible
for them because of the joints in the segments. Specially
sharp bending takes place at the articulation of the cephalothorax and the abdomen. In spite of specific peculiarities
of body structure among copepods, and the existence at all
stages of several methods of locomotion, we may observe that
at the time during their ontogenesis when more rapid swimming
by means of strokes of the abdomen in a horizontal plane is
developed, the breadth of the body, the position of the line
of greatest body width along the longitudinal axis, and various
other characteristics are altered according to the same rule
as applies to the corresponding structures among fishes
(Aleev, 1963). For example, as the entomostracans grow,
the difference in breadth of the parts of the body becomes
continuously greater, the lobes of the furcal fan of spinules
become more separated in the best swimmers, the body becomes
more compact and streamlined, the abdomen develops in a manner
similar to the caudal peduncle of a fish and the amplitude
of movement of the strokes of the abdomen increases (Table 2,
- 21 Fig. 2 and 3). All these characteristics permit more rapid
swimming and a decrease in water turbulence and in the resistance of the medium.
One of the most important parameters characterizing
the process of movement is the ratio of inertial force to
the force of viscosity, which can be expressed by the
Reynolds number (Re). 3
With increase in size and speed of
movement in animals [page 58] the Reynolds number increases
and consequently the importance of inertial force in the process of movement relative to the magnitude of the force of
viscosity also increases. For example, among the nauplii of
Acartia and Calanus it is very small and equal to 1.12 and
9.4 respectively, while among sexually mature Acartia and
especially Calanus it is much larger, being 18.0 and 307.8.
Comparing the life forms of Acartia and Calanus on
the basis of the characters enumerated above shows that Calanus
is a more accomplished and rapid swimmer than Acartia. Calanus
has become adapted to living in considerably deeper water and
to migrating periodically and rapidly from the deep layers to
the upper waters which are rich in food, and it is more effiL-- cient
than Acartia in its utilization of phytoplankton.
On the basis of what is given above we may now outline
the information on production and utilization of energy by
the populations of copepods studied, and also by the epiplanktonic and bathyplanktonic ecosystems as a whole.
Tables 3, 4 and 5 set forth the absolute magnitudes
and the relative rates for these processes. As was shown
3 Re = MIt where V is the rate of movement of the
current
or of the body in any medium, L is the length or breadth of the
moving current or body, and '1r is the kinematic viscosity of the
medium (Aleev, 1963). In the case at hand, at 15°C the
kinematic viscosity of sea water is taken to be 0.014.
- 22 -
[Pane 58]
Table 3 - Daily expenditure and accumulation of energy by populations
\
of Acartia and Calanus in the Black Sea by growth stages (in calories/m2 ).
e
Conepodites
I i v I III I
Nauplii
"
I
I
Second
2nd copepod- lst copepodite
ite life form I
life form
nauplial
life form
chursi
Increment
1;.etabolism
Ration
0,86
16,97 37.38
0 1,35 47,24
4,29
26,08
37,96
3,20 26,77 9,71
7,50
12,76 66,74 37,69 27,77
19,95 116,38 59,56 44,07
13,55
63,93
95,85
Calanus
hagoltuulkurs
Increment
Ration
13,76
52,14 114,07 47,52 23,98
70,40 524,48 876,90 381,52 107,45 30,96
7 3,20 . 508,08 1031,74 550,09 171,60 61,04
9,95
8,06
19,90
18,70
31,23
55,35
- 23 -
[Page 59]
Table 4 - Daily expenditure and accumulation of energy by populations of
Acartia and Ca lanus in the epiplanktonic anc32 bathyplanktonic ecosystems .
FTe-TI un-it for columns 4-9 is gram-ca lories/m . See page 5 for explanation
of the symbols .]
2
1
I
Species or grdups
Calanus
4
5
6
7
8
669,8
1020,0
(4;11:1u ndanee
ieeespri"9
pla nkt (Ale: systen.,
bay
E pi e1An rikto5nâ sysiem,
369882
903,1
147,3
167327
292,0
65,9
eathIpl 411 k.to n c Syeten
open s
23919
1911,6
epopian kbonic sish'em 3587407000
th a baj
16284,0
16602,0
n
/learn&
3
Phytoplankton
including
Epx p),1 n let on; c sysee n,
• 'open sea
106794000
1867,6
1514,0
Noctiluca
euthy plaillttonlesIstee
211486000
6375,0
4292,0
*peal sea
E pi p la nkt oni o
community
Bathyplanktonic
community
Including plant food.
Open sea
711,0*
289,3 444,0
' 378,0*
817,1
569,0*
355,2
301,0*
280,1 2031,0 2566,0*
2311,1'
2943,0
1025,0
9952,0
3938,0*
834,5*
- 24 -
earlier, the rapidly growing young copepod. ites of Calanus
take in energy twice as rapidly during the time of their growth
as do the young copepodites of Acartia. At the same time the
Calanus of the older age-groups use up accumulated energy
twice as intensively, during the time of their migration, as
do Acartia of the corresponding stages. Both of these relationships between accumulation and disposal of energy in the two
populations will depend on what the [page 60] age composition
of the population may be. During the period of our investigations at sea young individuals predominated in both populations. The average age of the Calanus population was somewhat
greater than that of the Acartia population, for the average
weight of an individual in the Acartia population lay between
copepodite stages I and II, while in the Calanus population
it lay between stages II and III. Although in Calanus the
average age of the population corresponded to a greater mean
daily growth than in Acartia (see Table 1), nevertheless in
Acartia the fraction of rapidly growing stages in the population (the ratio of the weight of rapidly growing stages to
the weight of the whole population) was considerably greater
(51.5%) than in Calanus (24%). As a result of this relationship between the weight and age composition of the populations
the coefficients of efficiency ( u ) and of relative rate (u)
of production of energy [i.e., increase in biomass] in the .
Acartia population were also higher than in the Calanus
population (see Table 5). We must however notice that the
difference between these coefficients in the two populations
was not very great (1.3-1.5 times).
The relative rate of energy metabolism (-5) was approximately the same in the Acartia and Calanus populations. This
shows that the Calanus population uses its energy for metabolism considerably more economically [ekonomnee] than the
Acartia population, in spite of the fact that it performs daily
vertical migrations of considerably greater amplitude and speed.
- 25 -
[Pace 60]
Table 5 - Indices of production and utilization of energy
by populations and communities of the epi- and bathyplanktonic systems in the western galistaza of the Black
Sea in June 1959. (All quantities are in calories/24-hr day).
(See page 5 for explanation of the symbols).
OP
B
Acartia
Calanus
Epiplanktonic
community
Bathyplanktonic
community
--17
P
U
R_
B
B
B
0,99 0,18 0,22
1,06 0,14 0,15
.i'..'
Pp
Pp
PP
_ 2.
flii
B'
B,
B ..
al
Pf
—B.,
ph
ph
Pf _
Eç
"
1,22 1,52 0,14
1,21 1,34 0,25
1,20 0,81 0,44 0,51 0,28
0,42 0,67 0,62 0,43 0,40
- 26 -
In comparing the Acartia and Calanus populations it
was revealed that the relative rate of utilization of energy
( E ) by Acartia [page 61] was 1.13 times as great as that by
Calanus. However the relative rate of intake of energy into
the population (E) in the two populations was the same (see
Table 5). This indicates that the Acartia population assimilated its food less completely [khuzhe] than the Calanus
population, and was apparently a greater contributor to the
formation of detritus.
If we compare the Calanus and Acartia populations in
respect to their efficiency in capturing (consuming) the mass
'
RI
(including Noctiluca) in the sea (B,
ofplantd
p ), it
Ph
appears that the Calanus population made use of
this food almost twice as effectively (see Table 5).
On the basis of preliminary data on the size of the
daily rations of all plant-eating organisms of the epiplanktonic and bathyplanktonic communities, the total phytoplankton
(plus Noctiluca) requirements of these animals has been computed. Assuming that in the Black Sea ecosystem here studied
all the phytoplankton production is consumed, the magnitude
of this production may be determined from the mass,of the
[H- re471.
phytoplankton eaten (the detritus used A in the upper levels
amounted to not more than 10% of the total phytoplankton)_.
The phytoplankton production estimated in this manner is to
be regarded as the actual, or real, production (P f ), which
is produced in the sea under concrete environmental conditions and a concrete regime of illumination; in contrast
to the potential, or possible, production of phytoplankton
(P ) determined by concrete conditions of illumination,
temperature, content of biogenic elements, existing abundance and natural mortality only, without taking consumption
into consideration. Referring each of these two values for
27 production to the biomass of phytoplankton (Noctiluca is
included in both production and biomass), and comparing the
coefficients obtained that characterize the relative rates
of potential( P p ) and actual ( P f ) production of phytoB Ph
1
B'Ph
plankton in the ecosystems, we see that important differences
exist between the two ecosystems. Inspite of the fact that
the rate of potential production of phytoplankton in the
epiplanktonic community is 1.2 times what it is in the
bathyplanktonic community (and if Noctiluca be excluded it
is 3 times as great), the relative rate of actual production
in the bathyplanktonic community is considerably greater (1.4
times as large) than in the epiplanktonic community (Table 5).
This difference between the epi- and bathyplanktonic ecosystems
is evident also in comparing potential and actual production
of phytoplankton with the biomass of the whole community
(see Table 5).
[page
62]
Conclusion
Analyzing the data obtained, the differences between
the Black Sea planktonic ecosystems in respect to their production and utilization of energy may be characterized as
regards their general features as follows.
The epiplanktonic ecosystem is distinguished by the
fact that the entomostracans of this system do not stray
outside the limits of phytoplankton accumulations, they
reproduce throughout the whole 24-hour day, and they also
consume phytoplankton around the clock; but being in warm
and well-lighted water they move a lot, though ineffectively,
throughout almost the whole of the 24 hours and hence for
practical purposes there is no daily storage of fat or
other organic matter.
- 28 -
Because of the continuous 24-hour consumption of
phytoplankton by the populations of epiplanktonic forms, the
actual production of this phytoplankton is low and it differs
greatly from the potential production. The potential productive capacity is therefore realized very incompletely -commonly to the extent of less than 20-55%.
This [actual
production] can be estimated from consumption in situations
where a large part or all of the algal production is consumed.
For example, the populations of two massively abundant species
of Acartia, in a bay and in the sea respectively, at different
seasons of the year consumed not more than 4-29% of the total
potential production of phytoplankton, expressed in calories,
each 24-hour day. Of the actual biomass of phytoplankton,
also expressed in calories, this magnitude of consumption
amounted to 4-23% (see Table 4). The populations of all
epiplanktonic Cladocera in the sea every 24 hours consumed
0.23% of the potential production and 0.35% of the actual
biomass of phytoplankton, expressed in calories; when compared
with the forms of phytoplankton they use (those of sizes up
to 8 p ) the corresponding figures become 0.5% and 9.5%
(Pavlova, 1967).
In the bathyplanktonic ecosystem the migratory entomostracans, mainly Calanus and the older stages of Pseudocalanus, are the principal users of phytoplankton, and they
ascend into the aggregations of phytoplankton only at night.
The maximum of division and growth of algal cells among the
principal species of phytoplankton takes place at various
hours during the lighted portion of the day; at night algal
division is suspended (Lanskaya, 1961). As a result of the
very small consumption which ordinarily takes place by day,
by herbivorous tiny young of these copepods and certain
epiplanktonic forms which have descended to deeper layers,
the phytoplankton reproduces rapidly and its actual production
(as estimated from the consumption of the algae) assuming little
mortality) more or less approximates the potential production.
In this case the consumption and hence the actual production
of the algae, expressed in calories, amount to more than
80-90% [page 63] of the potential production of the phytoplankton. The population of Calanus alone consumes up to 60%
of the potential production of phytoplankton expressed in
calories (Table 4) (Petipa, 1965).
Thus the bathyplanktonic plant-eating forms consume
phytoplankton in enormous quantities in order to form the
reserves of fat required for migration, and also to get the
matter and energy which are expended at night for reproduction,
that is, during several nocturnal hours almost the whole production is consumed. After descending into cold water these
entomostracans exist there in a passive condition, consuming
less energy for metabolism and consequently losing less weight.
In addition the energy which they conserve can supplement that
used for the production of eggs (McLaren, 1963).
Thus comparing data on the utilization of energy by
populations of abundant organisms, and by the plankton
communities as a whole, in the two ecosystems, we come to
the following conclusions.
The bathyplanktonic ecosystem is more efficient than
the epiplanktonic for the following reasons: actual production of phytoplankton approximates more closely to potential
production; and the food eaten by the entomostracans is
accumulated to a greater degree and is expended more economically. Considering these circumstances, we see that in
bathyplanktonic ecological systems where periodically migrating
species that spend part of the day in a passive condition
predominate among the first heterotrophic links, the energy
- 30 accumulated by producers under conditions otherwise equal is
more fully used by subsequent heterotrophic levels than in
epiplanktonic ecosystems having a predominance of non-migratory
species that are continuously in motion.
In general it may be said of both ecosystems that
with a decrease in the E coefficient (relative rate of potential production) of the phytoplankton, and with a shift in
the biomass of the whole community from the epiplanktonic to
the bathyplanktonic system, the actual utilization by zooplankton of the potential productive capacity of the phytoplankton increases. This increase is caused by the change
in the regime of elimination of phytoplankton (in particular,
its consumption), which makes for a higher actual production
of phytoplankton (Fig. 4).
To transfer the conclusions of the present work to
other ecosystems is possible on the basis of an understanding
of their life forms.
In other situations the species may be
different; however what is important is not knowing a list of
species, [page 64] but rather the life forms characterized by
particular adaptive features, which in turn are defined by some
particular capacity of the organisms to accumulate matter and
energy.
In using the method presented here, which employs both
field and experimental data, it is necessary to study all the
main species that make up a particular community.
For this it
is necessary to obtain complete information on the growth,
metabolism, rations, etc. for individual life forms under
the concrete conditions of their existence in the community.
This approach to the study of ecosystems will make it possible
to evaluate and compare different ecological systems. It must
be remembered that although the method proposed is laborious
[trudoemkii], yet it will provide the desired result, that of
- 31 -
[
Page 64
]
-4
46e,
--
\
a,
segeopa
Fig. 4 - Relation between the instantaneous rates of potential
and actual production of phytoplankton, and the biomass of
the community.
Abscissa - community biomass in kilocalories.
[See page 5 for symbols].
4
- 32 -
describing actual processes in the ecosystem. For quick preliminary and approximate evaluation of certain parameters of
ecosystems, "express" methods may also be used to advantage.
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