Hydrobiological Journal, 2014, Vol. 50, No.

Impact of Temperature Fluctuations on Embryonic-larval

Development of Esox lucius L. (Salmoniformes, Esocidae)†

V. A. Kuznetsov & S. V. Lukiyanov

University of Mordovia
Saransk, Russian Federation

Fluctuations of temperature within the limits of ecological norm were shown

to affect positively embryonic and larval development of Esox lucius L. In
optimal temperature regimes growth and development were accelerated,
survival rate of embryos and larvae increased (especially during the critical
periods of development), growth became more synchronous. Taking into
account high mortality of fishes and other poikilotherms in early ontogenesis,
optimization of their cultivation in variable temperature regimes can be one of
the main ways to increase efficiency of artificial reproduction.

KEYWORDS: embryonic-larval development, temperature, pike Esox

lucius, variable thermal regime, pre-larva, lineal growth.

Introduction

Most studies of embryonic-larval development of fishes and other poikilotherms as a rule in-
clude temperature-temporal regularities. Such approach is quite reasonable taking into account de-
pendence of the poikilotherms’ development rate on temperature, subjected to the Vant Goff’s rule
[2, 6]. In this concern effect of fluctuations of the environmental factors, particularly temperature,
on the embryonic-larval development of fishes is not sufficiently studied. Within the natural spawn-
ing areas development of the fish eggs and further larval development takes place under fluctuations
of the water temperature, pH, illumination and other environmental factors. For the eggs incubation
and cultivation of larvae constant optimal environmental parameters are recommended, though this
does not correspond natural conditions, with diurnal and seasonal fluctuations of abiotic factors.

Positive effect of the temperature oscillations on development and survival rate of the fish em-
bryos was noted in a series of studies. Thus, under variable temperature with amplitude 7oC duration
of embryonic development of Hucho hucho amounted to 33–45 days, survival – 73–95%, whereas
at the constant temperature 5.4oC – accordingly 60 days and 56% [30]. At incubation under the vari-
able thermal regime survival of Coregonus albula embryos was 1.4 times higher than under con-

†
Originally published in Gidrobiologicheskiy Zhurnal, 2013, Vol. 49, No. 5, pp. 67–79.

61 ISSN 0018-8166
©
2014 Begell House, Inc.
stant optimal temperature [32]. Mortality of Ptychohelius lucius embryos at the temperature
oscillations within 2.5o around optimal value decreased by 10–30%, and they turned to the external
feeding by 31 hour earlier, than at constant optimal temperature [28]. Diurnal temperature oscilla-
tions within 8–18oC positively affected development rate of the fish embryos of the families
Cyprinidae and Coregonidae and increased their survival rate [31].

It was shown [24] that normal development of the grass carp Ctenopharingodon idella embryos
needs variable temperature regime. It was also shown [9], that under temperature fluctuations
within the limits of ecological optimum body length of the weatherfish Misgurnus fossilis larvae in-
creases, survival of embryos and larvae of all development stages grows, frequency of abnormal
embryos occurrence decreases and pre-larvae hatch more bursting. Roe of the walleye Sander
vitreus was incubated at optimal temperature (10–11oC) and at gradual increase from 8.8 to 21.1oC;
in the latter case larvae hatched more early [33]. Variable temperature conditions were shown to be
more favorable for the embryonic development of pike and smelt Osmerus eperlanus, than constant
[17]. Earlier we stated positive effect of pH fluctuations on the embryonic-larval development of
pike [16]. In optimal variable regimes of pH growth and development rate increased, survival of
embryos and larvae also increased, especially over critical development stages.

Investigation of effects of the environmental factors variability on the embryonic-larval devel-

opment of fishes is not only of theoretical value, it is also important for intensification of artificial
fish reproduction. This is especially essential because embryonic-larval development determines
their further ontogenesis. It affects biology of mature fishes, determines their numbers and fertility,
productivity, peculiarities of reproduction cycles, distribution, migrations and possibilities of reset-
tlement into the water bodies with other hydrological regime.

Material and Method

Studies were carried out using pike Esox lucius Linnaeus (Teleostei, Salmoniformes,
Esocidae). It was chosen due to prolonged embryonic-larval development; at the spawn tempera-
ture (10oC) it lasts 36 days. Breeders were taken from the lakes Zaton and Dlinnoye (Mordovia,
Russian federation) over the spawning period and transferred to the laboratory, where in the same
day eggs were produced and fertilized. In each experimental series sexual products of the same pair
of breeders were used. Eggs were incubated in the Petri dishes under the constant temperatures 7.5,
8.5, 10.0, 11.5 and 12.5oC (accordingly lower and upper temperatures in the variable thermal re-
gimes). As constant optimum 10.0oC was accepted, at this temperature better survival of embryos,
maximal body length and mass and minimal yolk size at hatching were observed [25]. Effects of
variable thermal regimes were studied in the diapasons 8.5–11.5 and 7.5–12.5oC. In the first case
temperature fluctuations over incubation were within natural diapason, and in the second case – ex-
ceeded diurnal diapason. As reference we used periodical temperature measurements over embry-
onic development in the natural spawning area, were diurnal fluctuations amounted on average to
3.0–3.5oC. Besides, we used variable thermal regimes with periodic decrease (12 hours) 8.5–10.0
and 7.5–10.0°C, as a series of papers showed favorable effect of the temperature fluctuation within
moderate and low temperatures on the insects’ development [21]. Alternative temperature was
changes instantly twice a day. Each variant was twice or trice replicated. In the Petri dish 100 eggs
were placed at the fertilization stage, with developed perivitelline space and clearly expressed plas-

62
matic protuberance at the animal pole. Over incubation we deleted dead eggs and periodically regis-
tered development stages in 20 eggs.

After hatching pre-larvae were replaced to the thermostatic containers for studies of the further
larval development. The same constant and variable thermal regimes were used. Lineal dimensions
of pre-larvae were measured every 2 or 3 days. At the early stages (from cleavage to start of the
somitogenesis) observations were carried out using the MBA-1 microscope (magnification 7×8),
then – using the binocular loupe MBS-2 at magnification 2× or 4×.

Development stages of E. lucius were determined according to periodization of the embry-

onic-larval development, established by Yu. N. Gorodilov [5]. At each stage embryos’ and larvae’s
survival was assessed, as well as development rate and number of abnormal embryos. Beside abso-
lute parameters of the embryonic-larval development, also relative units were used: τ 0 – tau-zero
[6] and τ s – tau-somit-interval [4]. At different constant temperatures τ 0 was determined in a series
of the preliminary experiments, where 10 eggs’ samples from different breeders were used. After
fertilization 20 eggs were taken and constantly observed with interval 0.02–0.05 τ 0 until 4–6 cleav-
age furrows. Intervals between appearance of the further cleavage furrows in 3–4 advanced eggs
were registered. Value of τ 0 was calculated according to T. B. Rudneva’s formula [26]:

I 2− 4
τ0 = ,
2

where I2–4 – interval between appearance of furrows of the 2–4 divisions (minutes).

Tau-somit-interval (τ s ) was determined directly over the eggs’ incubation under different con-
stant and variable thermal regimes according to methods, described in [5]. Material was statistically
processed using the Microsoft Exñel.

Results and Discussion

In a series of preliminary experiments relative temporal parameters of the embryos’ and lar-
vae’s development under constant temperatures were determined: period from fertilization to ap-
pearance of the first cleavage furrow (τ fert ), duration of a mitotic cycle (τ 0 ) over period of
synchronous eggs’ cleavage and time of separation of one pair of somites over period of the syn-
chronous metamerization of the axial mesoderm (τ s ).

Considered parameters clearly depended on temperature, and our data are comparable with the
literature [5, 10]. Taking into account period of the temperature fluctuations (12 hours) it was not
possible to consider the first two parameter (τ fert and τ 0 ) under variable temperatures, so duration of
the larval development in terms of τ 0 was assessed in comparison with value of the parameter at
constant optimal temperature 10.0oC (τ 0 was equal to 90.4 ± 0.4 min). Time of separation of one
pair of somites over period of the synchronous metamerization of the axial mesoderm (τ s ) also de-
pended on temperature [4, 6]. This dependence on the constant temperature was studied in [5]. Our
data practically totally coincided with these results. However, somitogenesis is prolonged and un-
der variable temperatures this regularity is displayed in different way. Temperature fluctuations
over the eggs’ incubation reduced period of somitogenesis. This was noted under temperature fluc-
tuations around constant optimum and at its shift to lower values. To a greater extent this effect was

63
 Fig. 1. Number of somites in the pike’s embryos over period of the axial metamerizarion
under different thermal regimes: 1 – 10.0o; 2 – 8.5–10.0o; 3 – 7.5–10.0o; 4 – 7.5–12.5o; 5 –
8.5–11.5o.

revealed under thermal regime 8.5–11.5oC (Fig. 1), where time of the somites’ forming decreased
1.29 times as compared with incubation at constant 10.0oC.

As it was mentioned, dependence of the development rate of the pike’s embryos on constant
temperatures is quite well studied. In a series of the preliminary experiments it was revealed that op-
timal constant temperature, where maximal development rate and survival of embryos and pre-lar-
vae is registered, is 10.0oC, this meets literature data [25, 34]. So, just this temperature was
considered as control for variable thermal regimes.

In the first day of incubation, before start of somitogenesis, embryonic development rate of the
pike under variable thermal regimes was lower, than under constant temperature 10.0oC (Table 1).
This was connected with the fact that in the beginning of the experiment eggs were incubated under
low temperature and in 12 hours (fluctuation period) water was warmed to the appropriate higher
temperature.

Under temperature fluctuations within the limits 10.0 ± 1.5 and 10.0 ± 2.5oC differences in the
development rate became evident from period of the even somitogenesis. Temperature fluctuations
of 1.5o around constant optimum was revealed to be the most favorable – embryonic development
rate increased 1.26 times as compared with those under constant 10.0o (P < 0.001). Pre-larvae
hatched almost three days earlier, than under constant. Besides, embryonic development rate ex-
ceeded those under higher variable temperature (under 11.5oC time from incubation to hatching was
equal to 276.5 hours). Under more amplitude (10.0 ± 2.5oC) embryonic development also acceler-
ated, however it was somewhat lower than in the previous thermal regime (P < 0.01, 0.001). So,
temperature fluctuations within 3o were found to be the most favorable for the embryonic develop-
ment of E. lucius, this value corresponds to l fluctuations over embryogenesis in natural spawning
areas.

Stimulation of the embryonic development under temperature fluctuations can be confirmed by

data, obtained in lower temperatures (thermal regimes 7.5–10.0 and 8.5–10.0oC). In the beginning
of the experiment development rate under these regimes was lower, than under constant optimum,

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 Table 1

Rate of embryonic development of Esox lucius L. at optimal temperature (10.0oC) and under
variable thermal regimes (12 : 12 hours)

Duration of incubation (hours) after impregnation in

Development stages thermal regimes
10.0o 8.5–11.5o 7.5–12.5o 8.5–10.0o 7.5–10.0o
I – preparation to cleavage 0.0 0.0 0.0 0.0 0.0
II – cleavage 3.0 3.9 4.4 3.9 4.4
III – blastula 18.1 ± 20.2 ± 19.8 ± 20.7 ± 21.6 ±
0.1 0.1*** 0.1** 0.1*** 0.1***
IV – gastrula 34.7 ± 35.0 ± 35.3 ± 35.6 ± 36.1 ±
0.1 0.1 0.3 0.4 0.5
V – start of somitogenesis (2–3 73.2 ± 64.3 ± 62.8 ± 79.5 ± 83.8 ±
pairs of somites) 0.6 0.5** 0.5** 0.7 0.7***
VI – forming of the 1st branchial 119.0 ± 98.6 ± 104.1 ± 121.9 ± 123.6 ±
arch (27 pairs of somites) 0.6 0.6*** 0.5*** 0.7 0.8
VII – eyes pigmentation (43 pairs 146.4 ± 119.6 ± 129.4 ± 145.6 ± 149.7 ±
of somites) 0.8 0.7*** 0.7*** 0.8 0.9
VIII – forming of buds of the 171.1 ± 139.9 ± 149.9 ± 162.4 ± 169.5 ±
pectoral fins (56 pairs of somites) 0.9 0.7*** 0.8*** 0.8 0.9
IX – pre-hatching 201.3 ± 162.9 ± 184.9 ± 186.4 ± 197.2 ±
1.0 0.8*** 0.8** 0.8 1.0
X – start of hatching 289.9 ± 232.4 ± 264.6 ± 257.5 ± 278.6 ±
1.0 0.9*** 1.0*** 1.1*** 1.0
XI – mass hatching 311.5 ± 245.2 ± 282.7 ± 275.4 ± 299.0 ±
1.1 1.0*** 0.9*** 1.0*** 1.0
XII – end of hatching 330.9 ± 262.8 ± 300.8 ± 290.9 ± 315.8 ±
1.3 1.2*** 1.3*** 1.1*** 1.0*
Note. Here and in Table 2: * difference is statistically reliable at p < 0.05; ** difference is statisti-
cally reliable at p < 0.01; *** difference is statistically reliable at p < 0.001.

whereas to the end it increased and exceeded those under 10.0oC. In all considered thermal regimes
hatching was more bursting.

Higher development rate under variable temperature was supported by growth of survival. De-
velopment of fishes and other hydrobionts is known to include some critical stages, where signifi-
cant portion of embryos die [11]. Many eggs die over impregnation, first of all this depends on the

65
 Fig. 2. Mortality of Esox lucius eggs under considered thermal regimes (I – gastrula; II –
somitogenesis; III – hatching): 1 – 10.0o; 2 – 8.5–11.5o; 3 – 7.5–12.5o; 4 – 8.5–10.0o; 5 –
7.5–10.0o.

breeders’ quality. Stages of cleavage and gastrulation are even more sensitive, when elimination
can amount up to 40%. Period of the embryo forming and preparation to the hatching also are quite
important [19]. Minimal elimination of the pike embryos over the critical stages was registered un-
der variable thermal regimes (Fig. 2). In optimal variable regime 8.5–11.5oC embryos’ survival was
1.25 times higher than under optimal constant (P < 0.05). Similar pattern was noted in other variable
thermal regimes. No heterochronies in terms of the organs’ forming over the critical development
periods and no significant abnormalities of embryos in all constant and variable thermal regimes
were registered.

Periodical temperature fluctuations over incubation accelerated growth and development of the
pike pre-larvae. Maximal positive effect was registered at fluctuation within 1.5o around constant
optimum – development temp increased by 29.7% and growth rate by 10.7% (Table 2). Confidence
of difference of the pre-larvae body length and development time in variable and constant optimal
thermal regime exceeded 99.9%. Bigger fluctuations and even temperature decrease also favorably
affected larval development of pike: larvae’s growth and development rate increased. In optimal
variable thermal regimes stages of larval development and dimensions of the experimental speci-
mens exceeded those in constant temperature, for instance, in the thermal regime 8.5–11.5oC
pre-larvae grew and developed quicker than at constant temperature 11.5oC.

Optimization of the pike cultivation in the variable thermal regimes can be confirmed by data
on survival rate. In all variable thermal regimes this parameter was statistically higher, than under
constant optimum (see Table 2). Minimal elimination over the larval development was registered
under temperature fluctuations ± 1.5o. Also in this thermal regime variation coefficient of the
pre-larvae’s body length was twice as less than under constant 10.0oC (P < 0.001). Taking into ac-
count, that rate of variability of the fishes’ body length serves as criterion of their favorable habitat

66
 Table 2

Growth and development of pre-larvae of Esox lucius L. at optimal temperature (10.0oC) and
under variable thermal regimes (12 : 12 hours)

Development time Body Variation

Develop- Tempera- Survival from fertilization length, coeffi-
ment stages ture, oC rate, % mm X ± sx cient, Cv
hours τs /τ0
Hatching 10.0 80 330.9 ± 179.2 8.06 ± 0.29
1.3 0.01
8.5–11.5 84 262.8 ± 184.3 8.15 ± 0.21
1.2*** 0.01**
7.5–12.5 81 300.8 ± 183.0 8.12 ± 0.26
1.3*** 0.01
8.5–10.0 85 290.9 ± 186.0 8.13 ± 0.25
1.1*** 0.01
7.5–10.0 82 315.8 ± 186.1 8.14 ± 0.21
1.0* 0.01
Forming of 10.0 77 365.7 ± 198.0 10.86 ± 1.55
the branchial 1.2 0.02
petals with
8.5–11.5 82 286.9 ± 201.2 11.39 ± 1.20
capillary
1.1*** 0.02*
7.5–12.5 81 332.0 ± 202.0 11.12 ± 1.38
1.1*** 0.02
8.5–10.0 82 318.8 ± 203.7 11.13 ± 1.55
1.0*** 0.02
7.5–10.0 80 348.0 ± 205.1 11.04 ± 2.35
1.2* 0.03
Growth of 10.0 74 438.8 ± 237.6 12.14 ± 1.59
the branchial 1.0 0.02
petals
8.5–11.5 81 340.4 ± 238.7 12.98 ± 1.08
0.9*** 0.04***
7.5–12.5 79 393.7 ± 239.6 12.67 ± 1.07
0.9*** 0.02*
8.5–10.0 80 376.3 ± 240.6 12.70 ± 1.17
1.0*** 0.02*
7.5–10.0 78 401.2 ± 236.5 12.61 ± 1.11
1.0*** 0.02*

67
 Table 2 (continued)

Growth and development of pre-larvae of Esox lucius L. at optimal temperature (10.0oC) and
under variable thermal regimes (12 : 12 hours)

Development time Body Variation

Develop- Tempera- Survival from fertilization length, coeffi-
ment stages ture, oC rate, % mm X ± sx cient, Cv
hours τs /τ0
Forming of 10.0 71 479.5 ± 259.7 13.23 ± 2.04
dorsal and 1.1 0.08
anal fins
8.5–11.5 78 369.9 ± 259.3 14.28 ± 1.19
0.9*** 0.06***
7.5–12.5 76 425.6 ± 259.0 13.96 ± 1.43
1.0*** 0.06*
8.5–10.0 77 407.6 ± 260.1 14.03 ± 1.35
1.1*** 0.06**
7.5–10.0 75 436.1 ± 257.0 13.95 ± 1.00
1.0*** 0.05*
Forming of 10.0 68 503.9 ± 272.9 13.35 ± 1.72
the ventral 1.2 0.03
fins
8.5–11.5 77 390.1 ± 273.5 14.45 ± 0.95
0.8*** 0.02***
7.5–12.5 75 449.2 ± 273.4 14.14 ± 1.13
1.0*** 0.02**
8.5–10.0 74 428.4 ± 273.9 14.20 ± 1.17
1.1*** 0.02**
7.5–10.0 73 463.4 ± 273.1 14.10 ± 1.43
1.1* 0.02**
Growth of 10.0 64 585.3 ± 317.0 14.33 ± 1.81
the ventral 1.2 0.02
fins
8.5–11.5 76 451.4 ± 316.5 15.86 ± 0.90
1.0*** 0.02***
7.5–12.5 74 519.9 ± 316.4 15.25 ± 1.11
1.0** 0.02**
8.5–10.0 72 495.5 ± 316.7 15.62 ± 1.09
1.1*** 0.02***
7.5–10.0 71 538.4 ± 317.3 14.35 ± 1.24
1.1* 0.02**

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conditions, noted decrease of variability of the lineal dimensions under variable thermal regimes
additionally indicates that temperature fluctuations are more favorable for the embryonic-larval de-
velopment, than its stability.

Conclusion

Obtained results meet general concept on effect of fluctuations of the environmental factors on
development of the poikilotherms. Insects’ development was shown to be accelerated under vari-
able temperatures as compared with constant optimal temperature [18, 29]. Positive effect of tem-
perature and other environmental factors’ fluctuations was also revealed for different groups of the
hydrobionts: infusorians [7], crustaceans [3] and rotifers [15]. Fluctuations of temperature, pH, sa-
linity, illumination, dissolved oxygen content significantly accelerate growth and development, op-
timize energetic, improve physiological state of some aquatic invertebrates and fishes [4, 12, 14, 27,
29]. At this noted effects are caused by impact of different factors, this indicates not-specific re-
sponse of the organisms. So, it can be supposed that any environmental fluctuations within spe-
cies-specific norm favorably affect organisms, and just this astatic serves as environmental
optimum [13].

According to the E. S. Bauer’s concept [1], maintaining of imbalance with the environment
needs additional energy expenses, which are supported by hypercompensation and lead to excess
anabolism. Presence of the super-recovery phase is confirmed by a series of studies, considered
adaptive response of the organism to the moderate stimulus [8, 15]. On O.A. Zaprudnova’s opinion
[8], energy of elevated ion concentration gradients on the cell membrane, formed as a result of the
regulatory processes at adaptations, provides growth of the organism resistance and excess of the
anabolic processes. Periodical fluctuations of the environmental factors, particularly temperature,
lead to launch of the adaptation mechanisms, which force organism to adapt to the changing condi-
tions. Over the first ontogenesis stages these adaptations are displayed mainly at the biochemical
level [22]. It was stated, that “adjustment of the functional properties of enzymes to their maximal
effectiveness is one of the main mechanisms of the temperature adaptation of the poikilotherms’
metabolism… Probably, temperature-dependent value Km of the certain enzymes reflects general
physiological state of the developing organism under different temperature conditions” [23, p. 82].
The same effect is observed under the impact of other environmental factors. Even low content of
the toxic substances activate enzyme systems of the fish embryos and accelerate their development
rate [20]. So, importance of establishment of new forms of the stationary balance (environmental
adjustment) needs additional work, which is supported by acceleration of growth and development
due to hypercompensations. Results of our studies and literature data on effect of the environmental
factors fluctuations on the living organisms can be considered just from this viewpoint.

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