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18
Журнал Белорусского государственного университета. Экология. 2024;4:18–34
Journal of the Belarusian State University. Ecology. 2024;4:18–34
УДК 574.4
МОДЕЛИРОВАНИЕ РОСТА ИНВАЗИВНОГО ВИДА РЕЧНЫХ РАКОВ
PROCAMBARUS VIRGINALIS (DECAPODA, ASTACIDEA)
В РАЗЛИЧНЫХ ТЕМПЕРАТУРНЫХ УСЛОВИЯХ
А. П. ГОЛУБЕВ1), Е. А. УЛАЩИК1) , О. А. БОДИЛОВСКАЯ1)
1)Международный государственный экологический институт им. А. Д. Сахарова,
Белорусский государственный университет,
ул. Долгобродская, 23/1, 220070, г. Минск, Беларусь
У мраморного рака Procаmbarus virginalis определена зависимость длительности межлиночных интервалов от массы
тела и величины приростов массы тела за отдельные межлиночные интервалы в диапазонах температуры 15,3–17,9 °С;
7,5–18,9; 19,1–20,8; 21,0–22,8; 22,9–25,2 и 25,3–28,9 °С. По этим данным рассчитаны кривые роста их в указанных диа-
пазонах температур и суммы эффективных температур (Sef) у особей за периоды ювенильного роста и размножения.
Среднее значение Sef за ювенильный период P. virginalis (до достижения новорожденными особями массы тела 1,4 г)
в исследованных температурных интервалах составляет 4316 градусо-дней при температуре биологического нуля, рав-
ном 7,6 оС. Для периода размножения (до достижения массы тела от 1,4 г до предельной массы 15 г) 10630 градусо-дней
и 3,0 оС соответственно. По годовой динамике среднемесячных температур в шести континентальных водоемах в преде-
лах инвазивного ареала P. virginalis (Швеция, Беларусь, Германия, Словакия, Северная Македония и Малави) рассчитаны
значения Sef для периодов года, в течение которых возможен рост ювенильных и размножение половозрелых особей.
В водоемах умеренных широт, расположенных в Швеции, Беларуси, Германии и Словакии, значения Sef в период роста
ювенильных особей изменяются в пределах 1083–2099 градусо-дней. В более южном водоеме Северной Македонии
этот показатель достигает 2990, а в тропическом африканском водоеме в Малави – 7076 градусо-дней. Следовательно,
новорожденные особи P. virginalis, которые в водоемах умеренной зоны Европы отрождаются в первой половине лета,
способны достичь половой зрелости лишь в третье лето жизни, а в тропическом водоеме – уже в первое лето жизни.
Значения Sef для периодов года, благоприятных для роста половозрелых особей, в исследованных водоемах Европы
возрастают от 2031 (водоем в Швеции) до 4657 градусо-дней (водоем в Северной Македонии). В тропическом водоеме
Малави этот показатель достигает 8058 градусо-дней, то есть максимальная продолжительность жизни P. virginalis в нем
не превышает двух лет. Тем не менее, во всем ареале половозрелые особи P. virginalis способны произвести не более
2–5 кладок яиц за жизненный цикл.
Ключевые слова: биологические инвазии; температурный режим; речные раки; мраморный рак Procambarus
virginalis; скорость роста; инвазивный потенциал.
Благодарность. Исследования выполнены в рамках инициативной НИР «Скорость роста популяций инвазивных
и аборигенных видов речных раков в условиях Беларуси» (2023–2024 гг., № госрегистрации 20230739) и гранта Ми-
нистерства образования Республики Беларусь для студентов, магистрантов, аспирантов и молодых ученых «Эколого-
биологическая характеристика инвазивных видов десятиногих раков в природных климатических условиях Республи-
ки Беларусь» (2023 г., № госрегистрации 20230468).
Образец цитирования:
Голубев АП, Улащик ЕА, Бодиловская ОА. Моделирование
роста инвазивного вида речных раков Procambarus virginalis
(Decapoda, Astacidea) в различных температурных услови-
ях. Журнал Белорусского государственного университета.
Экология. 2024;4:18–34 (на англ.).
https://doi.org//10.46646/2521-683X/2024-4-18-34
For citation:
Golubev AP, Ulashchyk EA, Bodilovskaya OA. Modeling the
growth of the invasive river craysh species Procambarus
virginalis (Decapoda, Astacidea) under dierent temperature
conditions. Journal of the Belarusian State University. Ecology.
2024;4:18–34.
https://doi.org//10.46646/2521-683X/2024-4-18-34
Авторы:
Александр Петрович Голубев – доктор биологических
наук, доцент; профессор кафедры экологического монито-
ринга и менеджмента.
Екатерина Александровна Улащик – аспирант кафедры
экологического мониторинга и менеджмента.
Ольга Александровна Бодиловская – кандидат биологиче-
ских наук, доцент; доцент кафедры общей биологии и гене-
тики.
Authors:
Alexander P. Golubev, doctor of science (biology), docent;
professor at the department of environmental monitoring and
management.
algiv@rambler.ru
Ekaterina A. Ulashchyk, postgraduate student at the department
of environmental monitoring and management.
ulasikekaterina@gmail.com
Olga A. Bodilovskaya, PhD (biology), docent; associate professor
at the department of general biology and genetics.
_olga_iseu@tut.by
Изучение и реабилитация экосистем
The Study and Rehabilitation of Ecosystems
19
MODELING THE GROWTH OF THE INVASIVE RIVER CRAYFISH
SPECIES PROCAMBARUS VIRGINALIS (DECAPODA, ASTACIDEA)
UNDER DIFFERENT TEMPERATURE CONDITIONS
A. P. GOLUBEVa, E. A. ULASHCHYKa , O. A. BODILOVSKAYAa
aInternational Sakharov Environmental Institute, Belarusian State University,
23/1 Daŭhabrodskaja Street, Minsk 220070, Belarus
Corresponding author: A. P. Golubev (algiv@rambler.ru)
In the marbled craysh Procambarus virginalis, the dependence of the duration of inter-larval intervals on body weight
and the magnitude of body weight gains for individual inter-larval intervals in the temperature ranges 15.3–17.9 °С,
7.5–18.9, 19.1–20.8, 21.0–22.8, 22.9–25.2 and 25.3–28.9 °С was determined. The growth curves of individuals in these
temperature ranges and the sum of eective temperatures (Sef) of individuals during juvenile growth and breeding periods
were calculated from these data. The average Sef value for the juvenile period of P. virginalis (until newborn individuals
reach a body weight of 1.4 g) in the studied temperature ranges is 4316 degree·days at the biological zero temperature
of 7.6 °C. For the breeding period (until reaching the body weight from 1.4 g to the limit weight of 15 g) – respectively
10630 degree·days and 3.0 °C. Based on the annual dynamics of mean monthly temperatures in six continental water bodies
within the invasive range of P. virginalis (Sweden, Belarus, Germany, Slovakia, North Macedonia and Malawi), Sef values
were calculated for the periods of the year during which juvenile growth and reproduction of sexually mature individuals
are possible. In temperate water bodies located in Sweden, Belarus, Germany and Slovakia, Sef values during the juvenile
growth period vary between 1083 and 2099 degree·days. In the more southern body of water in Northern Macedonia,
this value reaches 2990 degree·days, and in the tropical African body of water in Malawi it reaches 7076 degree·days.
Consequently, newborn individuals of P. virginalis, which in water bodies of the temperate zone of Europe hatch in the
rst half of summer, can reach sexual maturity only in the third summer of life, and in a tropical water body – already in
the rst summer of life. Sef values for periods of the year favorable for the growth of sexually mature individuals in the
studied water bodies of Europe increase from 2031 degree·days (water body in Sweden) to 4657 degree·days (water body
in Northern Macedonia). In the tropical water body of Malawi, this gure reaches 8058 degree·days, i.e. the maximum
life span of P. virginalis in this water body does not exceed two years. Nevertheless, throughout the entire range, sexually
mature individuals of P. virginalis are capable of producing no more than 2–5 clutches of eggs per life cycle.
Keywords: biological invasions; river craysh; marbled craysh Procambarus virginalis; growth rate; invasive
potential.
Acknowledgements. The studies were conducted within the framework of the initiative research project «Growth rate
of populations of invasive and native species of river crayfish in the conditions of Belarus» (2023–2024, state registration
number 20230739) and the grant of the Ministry of Education of the Republic of Belarus for students, graduates and young
scientists «Ecological and biological characteristics of invasive species of ten-legged crayfish in natural climatic conditions
of the Republic of Belarus» (2023, state registration number 20230468).
Introduction
Invasion of animal and plant species into new geographic regions as a result of the inuence of numerous
natural (geological, climatic and biological) factors with the displacement of native species has always existed.
With the advent of man and the anthropogenic factors he created, the process of invasion began to accelerate more
and more and in the second half of the twentieth century it became a serious environmental problem in almost all
regions of the planet.
One of the striking examples among aquatic organisms is the massive penetration of alien species of craysh
(order Decapoda, infraorder Astacidea) of North American and Australian origin into water bodies of Europe,
Asia and Africa, caused almost exclusively by anthropogenic factors. It leads not only to a decrease in the number
and even complete displacement of native craysh species and the destruction of established biotic complexes of
inland water bodies, but also causes signicant material damage. For the period 2000–2020 economic losses from
invasion of various craysh species worldwide exceed 120 million dollars [1].
By the beginning of the 21st century, in many European countries, the number of invasive craysh species
reached and even exceeded the number of their native relatives [2]. In the current situation, a number of methods
and measures have been proposed for the conservation of native species of craysh, but their eectiveness raises
reasonable doubts [3; 4]. In the foreseeable future, it is possible to expect that invasive craysh in European water
bodies will become dominant not only in the number of species, but also in the number and biomass of popula-
tions. In this case, they will inevitably enter into intense competition with each other, the outcome of which is
currently impossible to predict.
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However, this question is of signicant scientic interest, since it will expand the understanding of the patterns
of transformation processes of the fauna of continental water bodies in the modern era under the inuence of glob-
al natural (climate changes, biological invasions) and anthropogenic (pollution of water bodies, changes in their
abiotic and biotic characteristics, etc.) factors.
One of the most aggressive species of invasive decapod craysh, rapidly spreading throughout the planet, is the
marbled craysh, Procambarus virginalis (family Cambaridae), popular among aquarists around the world [5].
Its distinctive feature is obligate parthenogenetic reproduction, which is a unique case in the infraorder Astacidea.
Special molecular genetic studies have established that all aquarium parthenogenetic individuals of marbled
craysh are triploid females, which originated from a single individual of the subtropical North American species
Procambarus fallax (Hagen, 1870) as a result of a genomic mutation [6]. Two sex X chromosomes in the chro-
mosome set of Procambarus virginalis are genetically completely identical, and the third has quite signicant
dierences from them [7]. Most likely, in one female P. fallax, as a result of a violation of meiosis, an egg cell with
two X chromosomes was formed, which was successfully fertilized by spermatozoon with an X-chromosome.
After the experimental establishment of reproductive isolation between P. fallax males and females of marbled
craysh, the latter was recognized as an independent species, Procambarus virginalis sp. nov. Lyko, 2017 [5]. Its
occurrence is a striking example of saltation, or quantum speciation [8].
The natural range of P. fallax covers only the basin of the small Satilla River in the states of Georgia and
Florida (USA). This species, like other Astacidea, is bisexual. However, recent molecular genetic studies have
revealed the presence of parthenogenetic females of P. virginalis in its natural populations. Therefore, along
with the ospring from the bisexual reproduction of P. fallax, they also contain clones originating from parthe-
nogenetic individuals of P. virginalis [9].
In North America, P. fallax is one of the most important objects of the aquarium animal trade [10; 11]. Ob-
viously, some batches of P. fallax, caught from natural reservoirs for sale in the USA and then in Europe, also
contained parthenogenetic individuals, which quickly spread among aquarists.
Since the beginning of the 21st century P. virginalis from aquaria, as a result of accidental or deliberate intro-
duction, has widely spread throughout the water bodies of many countries of the world with signicantly dierent
temperature conditions. In Europe, it is distributed from Belgium to Romania and from Sweden to Ukraine and
Croatia [12–15]. Beyond its borders, the marbled craysh has widely settled in numerous reservoirs of the low-
land part of the island of Madagascar [16]. It was also found in one of the lakes on the Japanese island of Hokkaido
[17], reservoirs in Taiwan [18], Israel [19], and an ornamental pond in Macau (China) [20].
One of the most important parameters determining the invasive potential of a particular species is the rate of
growth of their populations in comparison with that of closely related native species [21]. In turn, it is determined
by three important parameters: the survival rate of juveniles, the total fecundity of females during the life cycle,
and generation time [22]. The total fecundity of female craysh is quite easy to determine based on the results of
field population studies.
It is much more dicult to determine the generation time in natural populations of craysh. For rough esti-
mates, it can be equated to the duration of the juvenile period in females, i. e. the age at which they laid their first
clutch. However, most species of crustaceans have a long-life cycle (from 2–3 to 10 or more years), which does
not always allow for appropriate laboratory experiments.
However, the growth rate of all craysh species is determined by the frequency of their molts, which in turn
is largely determined by the temperature of the environment [23]. Using the noble craysh Astacus astacus as an
example, we developed a model for reconstructing the somatic growth of individuals based on the duration of in-
termolt intervals in individuals with dierent body weights and body weight increments during separate intermolt
intervals [24]. The results of calculations of A. astacus growth curves using this model showed good agreement
with the corresponding empirical data. Therefore, we used this method to simulate the growth processes of mar-
bled craysh over their life cycle.
The modern extensive invasive area of marbled craysh covers regions with dierent natural and climatic,
primarily temperature, conditions. One of the most important limiting environmental factors for craysh is the
temperature regime of water bodies, which has a signicant impact not only on their survival and seasonality
of reproduction, but also on the duration of embryogenesis and intermolt intervals [25]. Therefore, studying the
eect of temperature on the growth of marbled craysh individuals allows us to make predictive estimates of the
invasive potential of their populations in new habitat conditions.
Materials and methods
The studies were conducted in 2015–2022 on individuals from a laboratory culture of P. virginalis kept at
the International Sakharov Environmental Institute of Belarusian State University. The culture obtained from a
single maternal individual was, of necessity, located in a laboratory room that was poorly heated in winter and
strongly heated in summer. During the year, the temperature in it varied from 13–16 °C in December–February
Изучение и реабилитация экосистем
The Study and Rehabilitation of Ecosystems
21
and to 28–32 °C in July–August. However, this same circumstance made it possible to estimate the eect of the
temperature factor on the frequency of molting.
Newborns at the age of 2–3 weeks were seated individually in vessels with a volume of 1 liter. Then, as
they grew, they were transferred to larger aquariums with a water volume of up to 5 liters. All containers with
animals were checked at least 1–2 days to record the dates of individual molts and the laying of eggs on pleopods.
All individuals were weighed after each molt. For further analysis, we used only the duration of time intervals
between two successive molts, during which females did not lay eggs or bear young.
The water temperature in the vessels was determined daily. These data were used to calculate average
temperatures for individual intermolt intervals. The animals in the experiment were fed live larvae of the
chironomid Chirinomus sp. and Cladocera species Daphnia magna, supplied in abundance. At least twice a week,
a complete change of water was carried out in all containers.
The specic growth rate of individuals (r, time-1) for certain periods of time (τ1 – τ2) was calculated according
to (1):
(1)
where W2 and W1 are the weight of individuals at ages τ2 and τ1.
The Van’t Ho coecient values (Q10) for molting frequency (V = 1/Dm, day-1, where Dm is the duration of the
intermolt interval) for individual temperature ranges were calculated according to (2):
(2)
where V1 and V2 are the frequency of molts at temperatures t1 and t2.
All calculations are performed in the STATISTICA 8 software package.
The present-day wide invasive area of marble craysh covers various natural zones – from the tropics to the subarc-
tic regions. The temperature regime of reservoirs in these regions varies sharply, which has a signicant impact on the
processes of growth and reproduction of this species. We conducted a comparative analysis of the features of changes
in average monthly temperatures in six model reservoirs in dierent zones of the range of this species and the features
of the impact of their temperature regime on the growth of marbled craysh. The model reservoirs were:
1. A reservoir near the city of Jönköping in Southern Sweden, where the northern border of the invasive area
of P. virginalis currently lies [26].
2. Zaslavskaye reservoir near Minsk (Belarus). As of 2024, this species has not been found in natural reservoirs
of Belarus. However, in our country it is also a popular aquarium species and sold in specialized stores [27], which,
unfortunately, does not exclude its penetration into the natural environment. In addition, Zaslavskaye Reservoir is
located in the central part of Belarus, so its thermal regime is quite typical for reservoirs throughout the country.
3. A reservoir in Frankfurt am Main (Germany), since the marbled craysh was first discovered in natural
water bodies exactly in Germany [28].
4. A reservoir in Bratislava (Slovakia), since a stable population of this species was found near this city [29].
5. Plain Dojran Lake (North Macedonia), since currently the marbled craysh actively populates the water
bodies of the Balkan Peninsula [30].
6. Coastal zone of Monkey Bay on the extreme southwestern section of the shore of Nyasa Lake (Malawi,
East Africa). We took it for rough estimation of the temperature regime in freshwater bodies of the island of Mad-
agascar, which is the southern border of the modern invasive range of the marbled craysh [16]. Unfortunately,
we were unable to find the necessary data on the thermal regime of freshwater bodies on this island in publicly
available sources of information. However, since Madagascar and Malawi are located in the geographic region of
Southeast Africa there is every reason to believe that the temperature regimes of freshwater bodies of Madagascar
and Lake. Nyasa Lake are very similar.
Data on the temperature regime of the listed reservoirs are taken from the publicly available Internet resource
https://seatemperature.info/. Calculations of the sums of temperatures for separate periods of the year were carried
out in the computer program «Integral Calculator» https://www.integral-calculator.ru/.
Results and discussion
In all species of crustaceans the duration of intermolt intervals increases with increasing mass of individuals
and decreases with increasing temperature [31]. In our experiments, individuals grew and molted over a wide
temperature range. Therefore, to eliminate the inuence of the temperature factor on the dependence of the dura-
tion of intermolt intervals (Dm) on the mass of individuals (W), all available Dm values were distributed over six
temperature intervals in which the average temperatures during intermolt intervals changed by no more than 3 °C.
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Despite the rather signicant scatter of empirical data in all temperature intervals, the relationship between these
parameters in P. virginalis, as well as in other species of crustaceans, is well approximated by the power equation:
Dm = pWq, (3)
where p and q are empirical coecients, the parameters of which are presented in table 1.
In double logarithmic coordinates, equation (3) is transformed into a linear regression equation:
lgDm = lgp + qlgW. (4)
In graphical form, the dependence of Dm on W in dierent temperature intervals is presented in Fig. 1, and the
parameters of equation (1) for dierent temperatures are in table 1.
Due to the large range of variation in individual weights, both scales are presented in logarithmic coordinates.
The straight lines are the regression lines of equation (2), whose parameters are given in Table 1; the dashed line
is the 95 % signicance level.
Fig. 1. Dependence between of the duration of intermolt periods (Dm, days)
and body weight (W, g) before the previous molt in marbled craysh at dierent temperature intervals:
a) 15.3–17.1 °C; b) 17.5–18.9 °C; c) 19.1–20.8 °C; d) 21.0–22.8 °C; e) 22.9–25.2 °C; f) 25.3–28.9 °C
Изучение и реабилитация экосистем
The Study and Rehabilitation of Ecosystems
23
Table 1
Parameters of equation (3) of dependence of interlinear interval duration on body weight of marbled craysh
Temperature
range, °C
Average temperature,
оС
Weight range of individ-
uals, g pq r* Average of
15.3 –17.1 16.5 0.148–9.484 45.0 0.2871 0.6382 1.351
17.5–18 .9 18.2 0.064–6.950 41.8 0.2185 0.5481 1.295
19.1–20.8 19.7 0.063–6.650 34.0 0.3353 0.76 42 1.362
21.0 –22.8 22.0 0.200– 4.786 24.9 0.5480 0.7100 1.303
22.9–25.2 23.9 0.246–20.52 31.4 0.4275 0.7479 1.333
25.3–28.9 26.2 0.154 – 4.538 28.3 0.4478 0.7736 1.356
*Correlation coecient between lgDm and lgW in the equation (4)
It is important to note that as the body weight of individuals increases, the eect of temperature on the frequency
of their molts weakens (Fig. 2).
Fig. 2. Dependence between the Q10 coecient for the frequency of molts (1/Dm, day-1)
and the weight of marbled craysh individuals (W, g) in the interval 16.5–26.2 °C
The values of 1/Dm for the temperatures 16.5 °C and 26.2 °C were calculated using the corresponding equa-
tions (3), the parameters of which are given in Table 1.
An increase in the mass of decapod craysh, which have massive and hard outer integuments, occurs only in
the first few days after molting, until the new integuments harden. Therefore, the frequency of molting directly
determines the rate of weight growth of craysh.
The principle of calculating growth curves of individuals is as follows. In the Excel-2003 editor, a ta-
ble of 4 columns is built (Table 2). The first column contains the serial numbers of molts (i). The second
column contains the weights of individuals after the corresponding molt (Wi). The values of the post-molt
weight of individuals in any pair of subsequent (Wi+1) and previous molts (Wi) can be calculated by the
equation:
(5)
where β is the ratio of the mass of individuals after the subsequent molt to their weight after the previous molt,
expressed in fractions of unity:
(6)
In all temperature intervals, no statistically signicant dependence of β values on the weights of individuals
was established. Therefore, for further calculations we will use their averaged values for each temperature interval
(Table 1).
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Table 2
Example calculations of age curves of marbled craysh per life cycle at temperatures of 25.3–28.9 °C
Number of moult, ii Wi, г Di
days τ, days iiWi, г Di, days τ, days
12 3 4 12 3 4
00.007 3 0 14 0.500 21 138
10.010 4 4 15 0.675 24 162
20.013 4 8 16 0.915 27 189
30.018 512 17 1.240 31 220
40.024 518 18 1.682 35 255
50.032 624 19 2.281 40 295
60.044 731 20 3.092 46 341
70.059 839 21 4.193 53 394
80.080 948 22 5.686 60 455
90.109 10 58 23 7.710 69 524
10 0.147 12 70 24 10.455 79 603
11 0.200 14 84 25 14.177 91 693
12 0.271 16 100 26 19.224 104 797
13 0.368 18 118 27
Body weight of individuals after each successive molt (Wi) increases exponentially:
(7)
where Wo is the average weight of newborn P. fallax individuals, which, according to our data, is 0.007 g, i – is the
molting serial number.
The third column contains the values of the duration of the subsequent intermolt interval (Di) for a molted
individual with mass Wi, calculated according to (4). The fourth column records the total values of D with an
increasing total, which corresponds to the age of individuals (τ. days) after each successive molt. The age of
individuals in our calculations was limited to 780–820 days, which approximately corresponds to the maximum
duration of life expectancy of this species in the temperature range of 20–25 °C.
Growth curves for other temperature intervals were calculated in a similar way (Fig. 3).
Fig. 3. Parameters of equation (4) and calculated growth curves of Procambarus virginalis at dierent temperature intervals:
a) 15.3–17.1 °C; b) 17.5–18.9 °C; c) 19.1–20.8 °C; d) 21.0–22.8 °C; e) 22.9–25.2 °C; f) 25.3–28.9 °C
Изучение и реабилитация экосистем
The Study and Rehabilitation of Ecosystems
25
According to our data [32], individuals began to produce their first clutches already when they reached a body
weight of 0.85 to 1.2 g. A denite dependence of this indicator on temperature has not been established. However,
in the vast majority of cases, such clutches were unviable and the females quickly discarded them. Viable clutches
began to be produced by larger individuals, with a body weight of 1.4 g or more.
The calculated growth curves of P. virginalis in all temperature intervals are satisfactorily described by the
second-degree polynomial equation:
W
τ = aτ2 + bτ + C, (8)
where Wτ is the mass of individuals, g, τ is the age of individuals, days, a, b and С are empirical constants.
The parameters of equations (8) for dierent temperature intervals are presented in Fig. 3. Based on them, the
ages of individuals were calculated when they reached a mass of 1.4 g in these intervals, which corresponds to
the duration of the juvenile period (Dj). With an increase in temperature (t, °C), the Dj values of marbled craysh
decrease, and the specic growth rate (r, day-1) during the period of juvenile growth increases (Fig. 2). The rela-
tionship between r and t is linear:
r = −0.0123 + 0.0019 t. (9)
The value of t at which r = 0 is 6.4 °C. This temperature is the lower temperature limit for the growth of
juvenile marbled craysh (Fig. 4).
Fig. 4. Temperature dependence of the duration of the juvenile period of marbled craysh (Dj, day)
and the specic growth rate during this period (r, day-1)
The to value we obtained for the juvenile growth of marbled craysh is close to the results of R. Seitz, et al.
[31]. They experimentally raised newborn individuals of this species constant temperatures of 15 °C, 20 °C, 25 °C
and 30 °C until the age of 104–195 days. The value of to for the specic growth rate of individuals for the first
100 days of their growth, calculated by us based on the data of these authors, was 7.6 °C.
Consequently, the lower temperature limit for the growth of juvenile marbled craysh can be taken to be close
to 7 °C. From here, the sum of eective temperatures (Sef, degree ·days) for the juvenile period (Dj, day) of this
species can be calculated according to:
S
ef = Dj(t – to), (10)
where t is the average temperature for the juvenile period.
According to the results of our experiments, the average value of Sef for the juvenile period of marbled
craysh in dierent temperature intervals is 4316 degree·days. The average weight of newborn marbled
craysh is 7 mg, and the average weight of individuals that have begun to produce viable clutches is
1.4 g. Hence, the increase in the mass of individuals during the juvenile period is 1.39 g. Consequently,
the sum of eective temperatures required for an increase in the mass of juveniles by 1 g is equal to
4316 / (1.4 g – 0.007) 3 = 3098 degree·days.
We were unable to nd specic data on the growth or lifespan of marbled craysh in natural reservoirs in
the literature. According to our data, its lifespan in the laboratory at an average annual temperature close to
20 °C does not exceed 2–2.5 years, and its maximum weight reaches 15–20 g [32].
According to calculations using equation (8), the age of reaching a body weight of 15 g was reduced by
increasing temperature from 1349 to 707 days (Fig. 5). As for the juvenile period, an increase in the specic
26
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growth rate in mature females during the growth period from 1.4 to 15 g with increasing temperature, is
described by a linear function:
r = − 0,0006 + 0,0002t. (11)
Fig. 5. Temperature dependence of the age at which marbled craysh individuals reach
a body weight of 15.0 g (D, day) and the specic speed of sexually mature individuals (r, day-1)
From equation (11) it follows that the lower temperature limit for the growth of sexually mature marbled
craysh is 3 °C, which corresponds quite well to the available literature data. Thus, the survival rate of P. virginalis
in a natural reservoir in the Czech Republic over a 240-day period, entirely including the winter months, was
25 % [33]. Most of the deaths of individuals occurred precisely during the cold period of the year, when the water
temperature dropped to 2–3 °C. At the same time, all surviving individuals did not feed in winter, being motionless
and essentially in a state of suspended animation. The exit from it occurred only when the water warmed up in
April to 5–7 °C.
In individuals of this species kept from September to April in an outdoor pool, molting was observed even
when the water temperature in it dropped to 5.1–9.5 °C [34].
The value of the sum of eective temperatures for the growth period from 1.4 to 15 g in all temperature intervals
we studied averages 10 630 degree·days. Therefore, to increase the body weight of sexually mature individuals
by 1 g, a sum of eective temperatures equal to 10630: (15.0 – 1.4) ≈ 782 degree·days is required. Since the
frequency of molts in sexually mature individuals of marbled craysh is weakly dependent on temperature, with
Q10 in the range of 1.15–1.38 (Fig. 2), changes in temperature will have only a small eect on the growth rate of
sexually mature individuals.
If the temperature of the water in a reservoir for each day of the year (ti) is known, the annual sum of temperatures
(Ssum) of the water in it can be calculated by summing:
(12)
However, for the purposes of our research, it is important to know not only the annual sum of temperatures or
the average annual temperature, but also the nature of temperature changes throughout the year. However, in most
cases, there is no data on daily temperature values in water bodies or in their biotopes where craysh live. In this
case, the annual sum of temperatures can be determined with sucient accuracy from changes in average monthly
temperatures or even from temperatures for individual dates. However, it is desirable that these data cover all
seasons of the year or at least the ice-free period.
The curves of annual temperature changes in continental water bodies are not strictly symmetrical for many
natural and climatic reasons. The period of the year with maximum temperatures almost always occurs at the end
of July – the first half of August. In the reservoirs of the Southern Hemisphere, on the contrary, minimum tem-
peratures are observed during this period of the year. As an example, let’s look at the change in average monthly
temperatures in the Zaslavskaye reservoir (Table 3).
Annual changes in water temperature in it (t, °C), as in other model reservoirs, are well described by the pol-
ynomial equation of a 5th degree:
t = aτ5 + bτ4 + cτ3 + dτ2 + eτ + f, (13)
where τ is the serial number of the day in the year, counting from January 1st (τ = 1), a, b, c, d, e and f are empirical
constants.
Изучение и реабилитация экосистем
The Study and Rehabilitation of Ecosystems
27
Table 3
Parameters of equation (13) describing annual changes in water temperature (t, °C) in water bodies
within the invasion area of Procambarus virginalis during the year (τ, ordinal number of days counted from January 1st)
Water body, localisation Equation
Water body near Jönköping in Southern Sweden t = 1,4442E-10τ5 – 1,1117E-7τ4 + 2,5091E-5τ3 – 0,0012τ2 – 0,0513τ + 4,7388
Zaslavskaye reservoir near Minsk, Belarust = 1,3331E-10τ5 – 9,2227E-8τ4 + 1,6072E-5τ3 + 0,0002τ2 – 0,0837τ +
4,4737
Water body in Frankfurt am Main, Germany t = 1,0697E-10τ5 – 7,5621E-8τ4 + 1,3638E-5τ3 – 0,0233τ2 – 3,0963E-5τ +
4, 9113
Water body in Bratislava, Slovakia t = 1,2123E-10τ5 – 8,9101E-8τ4 + 1,7945E-5τ3 – 0,0006τ2 + 0,0097τ +
3,6998
Plain Dojran Lake, North Macedonia t = 9,2464E-11τ5 – 6,578E-8τ4 + 1,1323E-5τ3 + 0,0001τ2 + 0,0061τ
+ 5,2108
Monkey Bay of Nyasa Lake, Malawi,
East Africa
t = – 2,2873E-11τ5 +1,3447E -8τ4 – 7,9151E-7τ3 – 0,0005τ2 + 0,0445τ +
27,6135
The denite integral of function (13) in the range from τ =1st day (January 1) to τ = 365th days (December 31) is
the sum of active water temperatures (Ssum) in a reservoir for an astronomical year. The values of Ssum calculated in
this way dier from those determined, according to (12), by no more than 5 % in both directions. This accuracy is
quite acceptable for the purposes of this study, given the signicant uctuations in the average annual temperature
of water bodies in dierent years.
The lower temperature limits for the passage of individual stages of ontogenesis in craysh dier signicantly
(Fig. 5). The exact lower (τmin, day) and upper (τmax, day) boundaries of these intervals can also be calculated using
equation (13), using the to values for the corresponding stages of ontogenesis. Integrating equation (12) in the
range τmin – τmax allows one to determine the sum of temperatures over this range (Ssum).
However, for the rates of many biological processes in poikilothermic organisms, the most important factor
is not temperature as such, but eective temperature (Sef). It is equal to the dierence between the temperature of
the environment (t, °C) and the temperature of biological zero, or the lower temperature limit for the occurrence
of this process (to, °C).
Fig. 6. Changes in monthly temperatures in the Zaslavskaye reservoir in 2023 according to the data of the Internet resource
https://seatemperature.info/. The curve is the line of equation (13), the parameters of which are given in Table 3:
line a – lower temperature limit of growth of sexually mature individuals; line b – lower temperature limit of juvenile growth;
line c – lower temperature limit of embryonic development and growth of newborn individuals; line d – temperature
of the beginning of clutch emergence by females in natural water bodies of the temperate zone. Range AF – the period of the year
when growth of sexually mature individuals occurs. The BE range is the period of the year when juvenile growth occurs.
Range CD – the period of the year when embryonic development and growth of newborn individuals occurs
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The sum of eective temperatures for the period of the year (dτ = τmax – τmin) in which a certain stage of on-
togenesis occurs (Sef) can be calculated according to:
(14)
where Ssum is the sum of temperatures for the interval of the year in which a certain stage of ontogenesis occurs,
calculated by integrating function (5) in the interval from τmin to τmax, δτ is the duration of this interval (days),
to is the temperature of biological zero for a given stage of ontogenesis, °C.
However, females of the marbled craysh in water bodies of the temperate zone begin to lay eggs only after
the spring warms up of the water to 16 °C [33], which is signicantly higher than the to value for the embryonic
development of the marbled craysh, equal to 13.1 °C [34]. This circumstance must be taken into account when
calculating Sef according to (14) for time periods in water bodies in which embryonic development of marbled
craysh can actually occur. In this case, this period begins when the water temperature in the reservoir warms
up to 16 °C in the spring, and ends when it drops to 13 °C in the fall. In fact, this period of time is the breeding
period for marbled craysh in natural reservoirs.
In marbled craysh, the values of to for passing through dierent stages of life stages in ontogenesis de-
crease, and the duration and sum of eective temperatures for their passage, on the contrary, increase. Thus,
the duration of embryogenesis in him with an increase in temperature from 16–17 ° C to 26–27 °C is reduced
from 66–69 days to 21–24 days. The Sef values for the period of embryogenesis average 299 degree·days, and
the lower temperature threshold of embryonic development is 13.1°C. In juveniles with a body weight of up to
0.32 g, the lower temperature limit for molting occurs, i. e. body weight growth is the same – 13–14 °C. At the
same time, the upper temperature limit for the survival of developing embryos and newborn marbled individu-
als is a temperature of 27 °C [32].
The lower temperature limit for the growth of juvenile marbled craysh is 7 °C (Fig. 4), and for mature
individuals it decreases to 3 °C (Fig. 5). The age at which the marbled craysh reaches sexual maturity, even
at temperatures ranging from 20 to 26 °C, is at least 200 days, and the average value of the sum of eective
temperatures for this period reaches 4316 degree·days.
Therefore, the boundaries and duration of the periods of the year in which these processes can occur in
natural reservoirs, as well as the sum of eective temperatures in these periods, will vary signicantly (Fig. 6).
The parameters of equations (13), which describe the annual variation of temperatures in model reservoirs, are
given in Table 3.
The period of the year with temperatures favorable for embryonic development increases as one moves from
north to south (Fig. 6). However, temperatures of 27 °C and above are lethal for embryos and newborn juveniles
of marbled craysh [32]. Therefore, in freshwater bodies of the tropical island of Madagascar (an analogue of
which is Nyasa Lake), the embryogenesis of marbled craysh can occur only in the period from April to Octo-
ber, when the temperature in them drops below 27 °C.
On the other hand, the upper temperature limit for the existence of juvenile and mature individuals of this
species exceeds 30 °C, so they are able to grow in tropical waters throughout the year.
The boundaries of the passage of individual stages of ontogenesis in P. virginalis in model reservoirs and the
sum of eective temperatures for these periods are presented in Table 4. The shortest period of the year (only
70 days) with temperatures at which embryogenesis of the marbled craysh can actually occur occurs in the
reservoirs of the South Sweden. However, due to low summer temperatures, the Sef value for this period is only
166 degree·days, or 1.8 times lower than the Sef value required for the embryonic development of marbled
craysh.
Obviously, in such temperature conditions, complete development of clutches in one growing season is
impossible. Therefore, the possibility of reproduction of P. virginalis populations in the region of Southern
Sweden seems very doubtful. However, 13 specimens of marbled craysh were discovered in the small river
Märstaån near Stockholm [26]. However, these authors themselves express reasonable doubts about the ability
of this species to create sustainable populations in the waters of Southern Sweden. Most likely, the adult indi-
viduals they found in this river were brought there only once.
On the other hand, in the reservoirs of the city of Dnieper (Ukraine), egg-bearing females of P. virginalis were
found even at the end of October, when the water temperature dropped below 10 °C [35]. Most likely, their clutch-
es were swept out in late summer – early autumn, when the temperature of the reservoir still exceeded 13 °C. In
this case, at the end of October, P. virginalis eggs could already be in the stage of winter embryonic diapause, typ-
ical for craysh of the temperate zone. At the same time, the ability of eggs and embryos of the marbled craysh,
which is subtropical in its region of origin, to survive a long and cold winter period in water bodies of the tem-
perate zone remains unclear. In any case, we were unable to find information about the presence of egg-bearing
females of this species in the waters of Europe during the winter months.
Изучение и реабилитация экосистем
The Study and Rehabilitation of Ecosystems
29
Table 4
Boundaries of individual stages of ontogenesis in Procambarus virginalis
in natural water bodies and sums of eective temperatures for these periods
Water body, localisation
Sum tem-
peratures in
the reservoir
for the year,
degree·days
Boundaries period
of reproduction,
embryogenesis
and growth of
newborns*, days
The sum
of eective
temperatures
for this peri-
od, degree·-
days
Limits of
juvenile
growth
period*,
days
Sum of
eective
tempera-
tures for
this period,
degree·days
Limits of
growth peri-
od of sexu-
ally mature
individuals*,
days
Sum of
eective
tempera-
tures for
this period,
degree·days
Water body near
Jönköping in Southern
Sweden
3158 206 – 275
70 166 133 – 316
184 1083
1 – 20 и
100 – 365
286
2031
Zaslavskaye reservoir
near Minsk, Belarus 3442 163 – 275
113 543 105 – 307
203 1567 69 – 330
262 2493
Water body in Frank-
furt am Main, Ger-
many
4491 146 – 288
143 850 79 – 321
243 2099 1 – 365
365 3324
Water body in Bratisla-
va, Slovakia 4396 148 – 284
153 837 1 – 365
365 1841 1 – 365
365 3301
Plain Dojran Lake,
North Macedonia 5749 122 – 302
201 1550 53 – 329
279 2990 1 – 365
365 4657
Monkey Bay of Nyasa
Lake, Malawi, East
Africa
9613 110 – 300***
191 2129 1 – 365
365 7076 1 – 365
365 8518
*In the numerator – ordinal numbers of days of the year, counted from January 1st. The first digit is the day when the water temperature
in the reservoir reached 16 оС, the second – when it decreased to 13.1 оС; in the denominator – duration of the period of the year in this
temperature range.
**Until the body weight reached 15 g.
***Period of the year when water temperature did not exceed 27 °С.
Fig. 7. Annual changes in mean monthly temperature (t, °C) in freshwater bodies in dierent climate zones in 2023. Based on data from
https://seatemperature.info/. 1. Lake in Southern Sweden. 2. Zaslavskaye reservoir (Belarus). 3. A body of water in Frankfurt am Main
(Germany). 4. A water body in Bratislava (Slovakia). 5. Doiran Lake (Northern Macedonia). 6. Monkey Bay, Lake Nyasa (Malawi).
Line a – Lower temperature limit for growth of sexually mature individuals; line b – lower temperature limit for growth of juveniles;
line c – lower temperature limit for embryonic and neonatal growth; line d – temperature at which females begin to deploy their
clutches in natural waters of the temperate zone; line e – upper temperature limit for embryonic and neonatal growth
30
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In more southern reservoirs of Belarus, Germany, Slovakia and North Macedonia, the duration of the repro-
duction period of the marbled craysh is signicantly longer, and the Sef value in it exceeds the similar value for
embryonic development. Consequently, in these reservoirs, females are able to fully tolerate a clutch of eggs, and
the juveniles hatched from them can continue to grow for quite a long period of time.
An important limiting factor for natural populations of marbled craysh is the high mortality of juveniles in
winter. Thus, the survival rate of juveniles (average weight 0.9 g) in open concrete tanks in northeastern Estonia
from September 2011 to April 2012 was only 8 %. At the same time, the peak of mortality occurred in the coldest
months – January and February. In sexually mature individuals (average weight 2.1 g), under the same conditions,
survival rate reached 60 % [34].
However, even juveniles that have successfully overwintered in European water bodies are not able to reach
sexual maturity during the second growing season in their life cycle. To achieve sexual maturity, juvenile marbled
craysh require a Sef value of over 3000 degree·days. At the same time, the corresponding indicator for the growth
period of juveniles in water bodies of Belarus, Germany and Slovakia for the period of the year with temperatures
above 7 °C varies within the range of 1567–2099 degree·days (Table 5). The same figure in the warmer Lake
Dairen reaches almost 3000 degree·days. However, even if some individuals at the end of this period are able to
lay a viable clutch, then in the coming cold period of the year it will most likely die.
Consequently, as a result of the reservoirs of the temperate zone of Europe, newborn individuals of marbled
craysh are able to begin to reproduce only in the third year of life. According to our observations, female marbled
craysh never produced a repeat formula immediately after the juveniles emerged from the previous ones. Always
soon after the juveniles hatched from the eggs, the females molted shedding their exoskeleton with the remains of
hyaline filaments. They issued repeated egg clutch, and not always, only after another molt. In sexually mature
individuals, intermolt intervals, even at temperatures above 20 °C, are quite long – at least 25 days (Fig. 1). There-
fore, the second clutch during the growing season in natural reservoirs will develop at rapidly decreasing autumn
temperatures, which will negatively aect the survival of embryos.
Therefore, during their third growing season in the reservoirs of Germany and Slovakia, they will be able to
produce one clutch, and perhaps two clutches in the warmer reservoirs of the Balkan Peninsula.
In contrast to the reservoirs of Europe, in tropical reservoirs there is no cold period of the year, which limits the
growth of not only sexually mature, but also juvenile individuals. Therefore, newborn juveniles are able to reach
sexual maturity in them by the age of 200 days and produce up to 3–4 clutches in two seasons of the year with
temperatures favorable for embryonic development (below 27 °C).
Reproduction through parthenogenesis signicantly increases the invasive potential of the marbled craysh,
since theoretically a new invasive population can be founded by a single mature female that has produced at least
one viable clutch during its life cycle. In contrast, the establishment of invasive populations of bisexual craysh
species requires large enough groups of heterosexual individuals to increase the likelihood of their contacts during
the breeding season.
However, the reproductive capacity of marbled craysh is signicantly lower than that of bisexual species. In
our experiments [32], clutches were produced by no more than 50 % of sexually matured individuals kept in in-
dividual vessels. Moreover, up to 80 % of all clutches produced were non-viable. In most cases, breeding females
produced one viable clutch during their life cycle, and only in exceptional cases – two such clutches. These results
are quite consistent with the available literature data [36]. According to them, among female marbled craysh kept
by US aquarists, 38.5 % did not reproduce, 23.0 % produced only one clutch, and only 38.5 % produced several
clutches.
Therefore, low clutch viability and very high mortality of juveniles during the cold season signicantly reduce
the invasive potential of marbled craysh. Hence, its spread across Europe is signicantly lower than that of oth-
er North American invasive species: the signal craysh Pasifastacus leniusculus, the striped craysh Faxonius
(Orconectes) limosus, and the red swamp craysh Procambarus clarkii. The first two species originate from the
temperate zone of North America and are therefore well adapted to low winter temperatures. In contrast, the red
swamp craysh, like the marbled craysh, comes from the subtropics of North America.
The native area of the signal craysh in North America covers the extreme south of British Columbia (Cana-
da), the states of Washington, Oregon, Idaho and northern California (USA). It is not highly resistant to elevated
temperatures, which limits its ability to move into warmer subtropical regions. The optimal temperature for the
development of eggs of this species in articial conditions is 12–14 °C, at which their survival rate reaches 90–
98 %. For individuals under one year of age, an average annual temperature of 18 °C is considered optimal [37].
However, the maximum growth rate of individuals was noted at 23 °C [38].
In 1961, P. leniusculus was first introduced to Sweden and then to other European countries as a potential
aquaculture object [26], but it quickly began to spread to natural reservoirs. Now in Europe, among the invasive
species of craysh, the signal craysh has the most extensive range. It extends from Sweden, Finland and Great
Britain in the north, to Spain, Croatia and Greece in the south. At the southern border of its European range,
Изучение и реабилитация экосистем
The Study and Rehabilitation of Ecosystems
31
the signal craysh lives in colder mountain reservoirs. The eastern border of its range is Lithuania, Poland, the
Kaliningrad region of the Russian Federation and the Daugava River (Western Dvina) in Latvia, up to the city
of Daugavpils in close proximity to the border with Belarus. But in Belarus, despite long-term searches, signal
craysh has not been discovered.
On the other hand, low winter temperatures in natural reservoirs (up to 2–3 °C) do not block the growth of not
only adult individuals, but also juveniles of P. leniusculus. Thus, their newborn individuals raised in the laborato-
ry from July to May on running water coming from nearby Lake Mälaren (Central Sweden) reached an average
weight of 300 mg in October, and over 500 mg in May. At the same time, the water temperature from October to
May varied within 2–5 °C. The survival rate of juveniles during the entire period of the experiment reached 40 %
[39].
In water bodies of Poland, female of signal craysh reach sexual maturity at the end of the second growing
season (body size 8 cm, weight 16 g) and produce the first clutch of eggs, the young of which will hatch at the
beginning of the next growing season [40]. The lifespan of this species in natural reservoirs can lasts 10 years or
more. Therefore, females can produce as much as 7–8 clutches during their life cycle.
The striped craysh F. limosus is the first alien craysh species in Europe. Its maternal range includes the
northeastern United States and southeastern Canada. It was first introduced in 1890 to the east of the German
Empire (now the territory of Poland) with the aim of introducing it into natural reservoirs to compensate for the
sharp decline in the population of the native noble craysh A. astacus, which was the most important in Europe
commercial species, due to repeated pandemics of craysh plague [41]. Then striped craysh was repeatedly in-
troduced into reservoirs in dierent regions of Germany, Poland and France, and in the interwar years they were
even grown in aquaculture. However, due to its small size and robust outer covers, it was not in great demand on
the market.
From the areas of initial introduction and aquaculture, striped craysh quickly spread across numerous water
bodies in Europe. It currently ranges from the Atlantic coast of France to the Balkan Peninsula and from Italy to
Lithuania and Latvia. In Belarus F. limosus was first discovered in 1997 in the Black Gancha River (a tributary
of the Neman River) at the junction of the borders with Poland and Lithuania. In the period from 2003 to 2009, it
was recorded in several small rivers of the Western Bug basin. By 2016, this species had spread along the Shchara
River up to the city of Slonim, and later along the Viliya River (both tributaries of the Neman River) to the dam of
the Vileika Reservoir. In 2022, it was discovered in the Slepyanskaya water system of Minsk [42].
Striped craysh, compared to signal craysh, have a signicantly wider range of temperature tolerance. It
tolerates low winter water temperatures well. At the same time, the range of temperatures favorable for its growth
and development is quite wide – from 15 to 33 °C. Therefore, it was successfully acclimatized not only in Europe,
but also in much warmer Mexico.
In the reservoirs of the Czech Republic, female striped craysh lay eggs from the second half of April to the
first half of May. In a ow-through incubation unit, where the water temperature varied within 7–17 °C, the
duration of embryonic development averaged 46 days. Females hatched in the first half of summer reach sexual
maturity in the autumn of the same year with a minimum body size of 45 mm and a weight of 2.25 g [43] and will
begin to reproduce in the next growing season. Along with rapid growth and sexual maturation, the spinycheek
craysh is characterized by increased resistance to pollution of water bodies and low oxygen content in water.
Like the signal craysh P. clarkii, the striped craysh produces one clutch per growing season. Since the life
span of the latter does not exceed two to three years, it is capable of producing no more than two clutches during
its life cycle.
The maternal area of the red swamp craysh is northern Mexico, southern and southeastern United States. In
the USA, its cultivation began in the 19th century. Now this species is widely cultivated in China, Kampuchea,
Thailand, Ethiopia, Canada, Australia and New Zealand, and in recent decades – in Europe, primarily in Spain.
However, from craysh farms it penetrates everywhere into natural water bodies, thus becoming an additional risk
factor for native craysh.
The current range of P. clarkii in continental Europe extends from the Iberian Peninsula to Italy, Germany,
Austria and Poland. It is also found in the south of Great Britain, in Sicily, Sardinia, Corsica and the Balearic
Islands [44]. He also entered the river. Nile in Egypt [45], into reservoirs in the west of the Japanese island of
Hokkaido [46].
Despite its subtropical origin, the red swamp craysh is a highly eurythermic species, capable of existing in
a very wide range of temperatures. In reservoirs of Germany and Poland it survives at low winter temperatures
close to 2–3 °C, and in Egypt (lower reaches of the Nile River) in summer it exists at temperatures up to 26–29 °C.
Embryonic development in this species can occur in the range from 7 °C (150 days) to 31 °C (11–14 days) [45;
47].
The sum of eective temperatures (Sef) calculated by us based on the data of these authors for the embryonic
development of P. clarkii, equal to 270 degree·days, is close to that for the marbled craysh – 298 degree·days.
32
Журнал Белорусского государственного университета. Экология. 2024;4:18–34
Journal of the Belarusian State University. Ecology. 2024;4:18–34
However, the lower temperature threshold of embryonic development (to) in P. clarkii is signicantly lower than
in the marbled craysh – 9.0 and 13.1 °C, respectively.
In P. clarkii populations from water bodies of Europe and Japan, egg-bearing females appear in the second
half of summer, when water temperatures reach their maximum annual values [44; 46]. At temperatures ranging
from 20 to 25 °C, the duration of embryogenesis does not exceed three weeks. However, females continue to
carry hatched larvae until their third molt. According to laboratory experiments, the gestation period of larvae
at an average temperature close to 24.5 °C takes another 25 days [46]. If we assume that the lower temperature
limit for growth of P. clarkii larvae for the first three intermolt periods is the same as for embryonic development
(i. e. 9 оС), as established for P. virginalis [33], then the total sum of eective temperatures for the periods embry-
ogenesis and gestation of young by females is 270 + 388 = 658 degree·days.
Consequently, in water bodies of the temperate zone with a long autumn-winter period, females of P.clarkii,
taking into account the late timing of the hatching of juveniles, are capable of producing no more than one clutch
of eggs during the growing season. However, even juveniles that have switched to an independent lifestyle will
find themselves in conditions of constantly decreasing temperatures in the autumn-winter period, which will
signicantly reduce their growth rate and lengthen the juvenile period. Therefore, in the temperature conditions
of water bodies of the temperate zone, juveniles of this species reach the minimum size of sexually mature indi-
viduals (body size 60 mm) at the age of at least 5 months, i. e. will begin to reproduce in the next growing season.
The lifespan of P. clarkii in nature is usually no more than 3–4 years. Consequently, during its life cycle, its
females are capable of producing 2–3 clutches of eggs. In warmer water bodies of the subtropical and tropical
zones, there is no long autumn-winter period, and the age of reaching sexual maturity is reduced to three months.
In this case, females can produce two clutches during a long growing season.
In contrast to the above species, P. virginalis, although it has a fairly wide range in Europe, is found in only
a small number of water bodies. In some of them, only single adult individuals were found one time, the further
fate of which remained unknown. A number of populations of this species are also known that have existed for
quite a long time. They are found mainly in the southern parts of their range with a warmer climate and long
growing and breeding seasons. However, even in the warmer Doiran Lake on the Balkan Peninsula, the marbled
craysh reaches sexual maturity only in the third growing season, i.e. one year later than the signal and striped
craysh. Only on the tropical island of Madagascar can the growth of juvenile and mature female marbled craysh
continue year-round. Therefore, in a few years it not only spread throughout this island, but also became a com-
mon and even commercial species here [16].
One of the most important indicators of the invasive potential of alien species is the maximum instantaneous
rate of population growth (rmax). The higher the rmax, the faster the population size increases, which deprives the
population with a lower growth rate of food and biotopic resources [22]. The value of rmax can be approximately
calculated according to:
(15)
where α1 is the survival rate of newborn females in the juvenile period, expressed in fractions of unity, α2 is the
proportion of breeding females in the total number of sexually mature individuals, F is the average number of
juveniles born by females during the life cycle, T is the generation time in the population.
The craysh generation time (T) can be approximately taken equal to:
(16)
where T1 and Td are the average age of females when they lay their first and last clutches in years. Td usually
corresponds to the maximum lifespan of females under natural conditions.
Fecundity (F) of the listed North American invasive crustacean species is quite comparable. In females of the
maximum age and maximum size, it reaches 300–500 eggs. The sex ratio in natural craysh populations is close
to 1:1, hence α2 ≈ 0.5. The only exception is the parthenogenetic marbled craysh, all individuals of which are
females, i. e. theoretically it has α2 = 1.0. However, since not all sexually mature females in this species produce
viable ospring, the real values of α2 in its natural populations are most likely signicantly lower. The survival
rate of all types of craysh in the juvenile period (α1) in natural reservoirs is very low, usually no more than 0.01–
0.05. Logarithm of the values of α1, α2 and F in (15) largely eliminates even their signicant (up to 3–5 times)
dierences in dierent craysh species.
Conclusion
Based on (15), the generation time (T) has a signicantly stronger eect on rmax for craysh populations than
other parameters of the life cycle of the individual. The shorter T, the higher the growth rate of their populations.
In water bodies of the temperate zone with a long autumn-winter season periods with low winter temperatures,
Изучение и реабилитация экосистем
The Study and Rehabilitation of Ecosystems
33
slowing down or even blocking the processes of embryonic development and growth of female craysh, the latter
are capable of producing no more than one clutch of eggs per life cycle.
In such circumstances the signal, striped and red swamp craysh, which begin to reproduce already in the
second growing season, will have an undoubted advantage not only over the native European noble craysh A. as-
tacus, narrow-clawed craysh Astacus leptodactylus, white-clawed craysh Austropotamobius pallipes and stone
craysh Aus. torrentium, but also invasive marbled craysh, which begin to reproduce 2–3 years later.
This conclusion is conrmed by numerous examples. In Belarus, the striped craysh is gradually replacing
the long-clawed craysh [48]. The signal craysh in Sweden and Finland displaces the broad-clawed and long-
clawed craysh [49], in the UK – the white-clawed craysh [50], and in Germany – the stone craysh [51]. And
such examples are far from unique.
In the foreseeable future, invasive craysh species in Europe will enter into intense competition with each
other, the outcome of which is currently dicult to predict. However, it is quite possible to predict it if, using the
model we have developed, we determine the temperature limits for embryonic development, growth and repro-
duction of individuals and the sum of eective temperatures for passing through these stages of ontogenesis.
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Статья поступила в редколлегию 12.09.2024.
Received by editorial board 12.09.2024.