ArticlePDF Available

Modeling the growth of the invasive river crayfish species Procambarus virginalis (Decapoda, Astacidea) under different temperature conditions

Authors:
  • International Sakharov Environmental Institute of Belarusian State University

Abstract

In the marbled crayfish 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 effective 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 first half of summer, can reach sexual maturity only in the third summer of life, and in a tropical water body – already in the first 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 figure 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.
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 craysh species Procambarus
virginalis (Decapoda, Astacidea) under dierent 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 craysh 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 eective 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 craysh; marbled craysh 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 inuence 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 craysh
(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 craysh species and the destruction of established biotic complexes of
inland water bodies, but also causes signicant material damage. For the period 2000–2020 economic losses from
invasion of various craysh species worldwide exceed 120 million dollars [1].
By the beginning of the 21st century, in many European countries, the number of invasive craysh 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 craysh, but their eectiveness raises
reasonable doubts [3; 4]. In the foreseeable future, it is possible to expect that invasive craysh 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.
20
Журнал Белорусского государственного университета. Экология. 2024;4:18–34
Journal of the Belarusian State University. Ecology. 2024;4:18–34
However, this question is of signicant scientic 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 inuence 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 craysh, rapidly spreading throughout the planet, is the
marbled craysh, 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
craysh 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 signicant
dierences 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
craysh, 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 ospring 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 signicantly dierent
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 craysh 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 craysh is quite easy to determine based on the results of
field population studies.
It is much more dicult to determine the generation time in natural populations of craysh. 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 craysh 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 craysh 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 dierent 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 craysh over their life cycle.
The modern extensive invasive area of marbled craysh covers regions with dierent natural and climatic,
primarily temperature, conditions. One of the most important limiting environmental factors for craysh is the
temperature regime of water bodies, which has a signicant impact not only on their survival and seasonality
of reproduction, but also on the duration of embryogenesis and intermolt intervals [25]. Therefore, studying the
eect of temperature on the growth of marbled craysh 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 eect 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 specic 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 coecient 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 craysh 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 signicant 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 dierent zones of the range of this species and the features
of the impact of their temperature regime on the growth of marbled craysh. 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 craysh 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 craysh 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 craysh [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 inuence 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.
22
Журнал Белорусского государственного университета. Экология. 2024;4:18–34
Journal of the Belarusian State University. Ecology. 2024;4:18–34
Despite the rather signicant 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 coecients, 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 dierent temperature intervals is presented in Fig. 1, and the
parameters of equation (1) for dierent 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 % signicance level.
Fig. 1. Dependence between of the duration of intermolt periods (Dm, days)
and body weight (W, g) before the previous molt in marbled craysh at dierent 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 craysh
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 coecient between lgDm and lgW in the equation (4)
It is important to note that as the body weight of individuals increases, the eect of temperature on the frequency
of their molts weakens (Fig. 2).
Fig. 2. Dependence between the Q10 coecient for the frequency of molts (1/Dm, day-1)
and the weight of marbled craysh 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 craysh, 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 craysh.
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 signicant 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).
24
Журнал Белорусского государственного университета. Экология. 2024;4:18–34
Journal of the Belarusian State University. Ecology. 2024;4:18–34
Table 2
Example calculations of age curves of marbled craysh 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 dierent 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 denite 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 dierent 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 craysh
decrease, and the specic 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 craysh (Fig. 4).
Fig. 4. Temperature dependence of the duration of the juvenile period of marbled craysh (Dj, day)
and the specic growth rate during this period (r, day-1)
The to value we obtained for the juvenile growth of marbled craysh 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 specic 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 craysh can be taken to be close
to 7 °C. From here, the sum of eective 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
craysh in dierent temperature intervals is 4316 degree·days. The average weight of newborn marbled
craysh 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 eective 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 specic data on the growth or lifespan of marbled craysh 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 specic
26
Журнал Белорусского государственного университета. Экология. 2024;4:18–34
Journal of the Belarusian State University. Ecology. 2024;4:18–34
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 craysh individuals reach
a body weight of 15.0 g (D, day) and the specic 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
craysh 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 eective 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 eective temperatures equal to 10630: (15.0 1.4) 782 degree·days is required. Since the
frequency of molts in sexually mature individuals of marbled craysh 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 eect 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 craysh live. In this
case, the annual sum of temperatures can be determined with sucient 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 denite 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 dier 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 signicant uctuations in the average annual temperature
of water bodies in dierent years.
The lower temperature limits for the passage of individual stages of ontogenesis in craysh dier signicantly
(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 τminτmax 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 eective temperature (Sef). It is equal to the dierence 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
28
Журнал Белорусского государственного университета. Экология. 2024;4:18–34
Journal of the Belarusian State University. Ecology. 2024;4:18–34
The sum of eective temperatures for the period of the year (dτ = τmaxτmin) 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 craysh 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 signicantly higher than the to value for the embryonic
development of the marbled craysh, 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
craysh 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 craysh in natural reservoirs.
In marbled craysh, the values of to for passing through dierent stages of life stages in ontogenesis de-
crease, and the duration and sum of eective 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 craysh is 7 °C (Fig. 4), and for mature
individuals it decreases to 3 °C (Fig. 5). The age at which the marbled craysh 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 eective
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 eective temperatures in these periods, will vary signicantly (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 craysh [32]. Therefore, in freshwater bodies of the tropical island of Madagascar (an analogue of
which is Nyasa Lake), the embryogenesis of marbled craysh 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 eective 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 craysh 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
craysh.
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 craysh 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 craysh of the temperate zone. At the same time, the ability of eggs and embryos of the marbled craysh,
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 eective 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 eective
temperatures
for this peri-
od, degree·-
days
Limits of
juvenile
growth
period*,
days
Sum of
eective
tempera-
tures for
this period,
degree·days
Limits of
growth peri-
od of sexu-
ally mature
individuals*,
days
Sum of
eective
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 dierent 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
Журнал Белорусского государственного университета. Экология. 2024;4:18–34
Journal of the Belarusian State University. Ecology. 2024;4:18–34
In more southern reservoirs of Belarus, Germany, Slovakia and North Macedonia, the duration of the repro-
duction period of the marbled craysh is signicantly 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 craysh 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
craysh 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
craysh are able to begin to reproduce only in the third year of life. According to our observations, female marbled
craysh 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 aect 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 signicantly increases the invasive potential of the marbled craysh,
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 craysh
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 craysh is signicantly 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 craysh 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 signicantly reduce
the invasive potential of marbled craysh. Hence, its spread across Europe is signicantly lower than that of oth-
er North American invasive species: the signal craysh Pasifastacus leniusculus, the striped craysh Faxonius
(Orconectes) limosus, and the red swamp craysh 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 craysh, like the marbled craysh, comes from the subtropics of North America.
The native area of the signal craysh 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 articial 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 craysh, the signal craysh 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 craysh 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
craysh 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 craysh 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 craysh F. limosus is the first alien craysh 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 craysh A. astacus, which was the most important in Europe
commercial species, due to repeated pandemics of craysh plague [41]. Then striped craysh was repeatedly in-
troduced into reservoirs in dierent 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 craysh 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 craysh, compared to signal craysh, have a signicantly 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 craysh 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
craysh is characterized by increased resistance to pollution of water bodies and low oxygen content in water.
Like the signal craysh P. clarkii, the striped craysh 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 craysh 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 craysh farms it penetrates everywhere into natural water bodies, thus becoming an additional risk
factor for native craysh.
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 craysh 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 eective 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 craysh – 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 signicantly lower than
in the marbled craysh – 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 eective 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
signicantly 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
craysh reaches sexual maturity only in the third growing season, i.e. one year later than the signal and striped
craysh. Only on the tropical island of Madagascar can the growth of juvenile and mature female marbled craysh
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 craysh 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 craysh populations is close
to 1:1, hence α2 ≈ 0.5. The only exception is the parthenogenetic marbled craysh, 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 ospring, the real values of α2 in its natural populations are most likely signicantly lower. The survival
rate of all types of craysh 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 signicant (up to 3–5 times)
dierences in dierent craysh species.
Conclusion
Based on (15), the generation time (T) has a signicantly stronger eect on rmax for craysh 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 craysh, 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 craysh, which begin to reproduce already in the
second growing season, will have an undoubted advantage not only over the native European noble craysh A. as-
tacus, narrow-clawed craysh Astacus leptodactylus, white-clawed craysh Austropotamobius pallipes and stone
craysh Aus. torrentium, but also invasive marbled craysh, which begin to reproduce 2–3 years later.
This conclusion is conrmed by numerous examples. In Belarus, the striped craysh is gradually replacing
the long-clawed craysh [48]. The signal craysh in Sweden and Finland displaces the broad-clawed and long-
clawed craysh [49], in the UK – the white-clawed craysh [50], and in Germany – the stone craysh [51]. And
such examples are far from unique.
In the foreseeable future, invasive craysh species in Europe will enter into intense competition with each
other, the outcome of which is currently dicult 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 eective temperatures for passing through these stages of ontogenesis.
References
1. Kouba A, Oficialdegui FJ, Cuthbert RN, Kourantidou M, South J, Tricarico E, Gozlan RE, Courchamp F, Haubrock PJ. Identifying
economic costs and knowledge gaps of invasive aquatic crustaceans. Science of the Total Environment. 2022;813:152‒325.
2. Holdich DM, Reynolds JD, Souty-Grosset C, Sibley PJ. A review of the ever-increasing threat to European crayfish from non-
indigenous crayfish species. Knowledge and Management of Aquatic Ecosystems. 2009;11:394–395.
3. Gherardi F. et al. Managing invasive crayfish: is there a hope? Aquatic Sciences. 2011;73(2):185–200.
4. Kozák P, Füreder L, Kouba A, Reynolds J, Souty-Grosset C. Current conservation strategies for European crayfish. Knowledge
and Management of Aquatic Ecosystems. 2011; 401:01–08.
5. Lyko F. The marbled crayfish (Decapoda: Cambaridae) represents an independent new species. Zootaxa. 2017;4363(4):544–552.
6. Martin P, Dorn NJ, Kawai T, van der Heiden C. The enigmatic Marmorkrebs (marbled crayfish) is the parthenogenetic form of
Procambarus fallax. Contributions to Zoology. 2010;79(3):107–118.
7. Gutekunst J,Andriantsoa R, Falckenhayn C, Hanna K, Stein W, Rasamy J, Lyko F. Clonal genome evolution and rapid invasive
spread of the marbled crayfish. Nature Ecology and Evolution. 2018;2:567–573.
8. Stegnij VN. Arhitektonika genoma, sistemnye mutacii i evolyuciya. Novosibirsk: Izdatel’stvo NGU; 1993. 143. Russian.
9. Gutekunst J, Maiakovska O, Hanna K, P Provataris P, Horn H, Wolf S, Skelton CE, Nathan J, Dorn NJ, Lyko F. Phylogeographic
reconstruction of the marbled crayfish origin. Communications Biology. 2021;4:1096.
10. Chucholl C. Invaders for sale: Trade and determinants of introduction of ornamental freshwater crayfish. Biological Invasions.
2013;15:125–141.
11. Faulkez Z. Marmorkrebs (Procambarus fallax f. virginalis) are the most popular crayfish in the North American pet trade. Knowl-
edge and Management of Aquatic Ecosystems. 2015;416:20.
12. Bohman P, Edsman L, Martin P, Scholtz G. The first Marmorkrebs (Decapoda: Astacida: Cambaridae) in Scandinavia. BioInva-
sions Records. 2013;2(3):227–232.
13. Kouba A, Petrusek A, Kozák P. Continental-wide distribution of crayfish species in Europe: update and maps. Knowledge and
Management of Aquatic Ecosystems. 2014;413:5‒31.
14. Novitsky RF, Son MO. The first records of Marmorkrebs [Procambarus fallax (Hagen, 1870) f. virginalis] (Crustacea, Decapoda,
Cambaridae) in Ukraine. Ecologia Montenegriana. 2016;5:44–46.
15. Dobrović A, Maguire I, Boban M, Grbin D, Sandra Hudina S. Reproduction dynamics of the marbled crayfish Procambarus
virginalis Lyko, 2017 from an anthropogenic lake in northern Croatia. Aquatic Invasions. 2021;16(3):482–498.
16. Andriantsoa R, Tönges S, Panteleit J, Theissinger K, Carneiro VC, Rasamy J, Lyko F. Ecological plasticity and commercial im-
pact of invasive marbled crayfish populations in Madagascar. BMC Ecology. 2019;19(8):1–10.
17. Kawai T, Takahata M. The Biology of Freshwater Crayfish. Natural history. 2010;2:3‒119.
18. Charlier P. Mutant invasive crayfish found infesting ponds in Taipei City park. [Internet, cited 2024 March 11]. Available from:
https://taiwanenglishnews.com/mutant-invasive-crayfish-found-infesting-ponds-in-taipei-city-park/.
19. Yanai Z, Guy-Haim T, Kolodny O, Levitt-Barmats Y, Mazal A, Morov AR, Sagi A, Noa Truskanov N, Milstein D. An over-
view of recent introductions of non-native crayfish (Crustacea, Decapoda) into inland water systems in Israel. BioInvasions Records.
2024;13:195–208.
20. Lam A. Foreign species of crayfish, hazardous to local ecology, found in Ttaipa. [Internet, cited 2024 March 20]. Available from:
https://macaudailytimes.com.mo/foreign-species-of-crayfish-hazardous-to-local-ecology-found-in-taipa.html.
21. Crandall KA. Procambarus fallax. The IUCN Red List of Threatened Species 2010 Crandall. [Internet, cited 2024 March 22].
Available from: http://www.iucnredlist.org/details/153961/0.
22. Pianka ER. Evolutionary ecology. 7th edition. [Internet, cited 2024 March 26]. Available from: https://books.google.by/books?id=-
giFL5bonGhQC&pg=PA1&hl=ru&source=gbs_toc_r&cad=2#v=onepage&q&f=true.
23. Hmeleva NN, Golubev AP. Produkciya kormovyh i promyslovyh rakoobraznyh. Minsk: Science and technology; 1984. 216 p.
Russian.
24. Golubev AP, Ulashchik EA. Mathematical modelling of the processes of continuous growth of the noble crayfish Astacus astacus
(Decapoda, Astacidae) under aquaculture conditions. In: Actual problems of wildlife protection in Belarus and neighbouring regions:
proceedings of the II International Scientific and Practical Conference. Minsk: [publisher unknown]; 2022. p. 106–112. Russian.
25. Khmeleva N, Golubev A. La production chez les Crustacès. Rôle dans les ècosystémes et utilizations. Brest (France): Institut
Francais de Recherche pour l’Exploitation de la Mer; 1986. p. 198. French.
26. Bohman P, Edsman L. Marmorkräftan i Märstaån. Riskanalys och åtgärdsförslag. Aqua reports. 2013; 17: 1‒115.
Журнал Белорусского государственного университета. Экология. 2024;4:18–34
Journal of the Belarusian State University. Ecology. 2024;4:18–34
27. Ulashchyk K, Zhu Y. The aquarium pet trade as a source of potentially invasive crayfish species in Belarus. In: Actual environ-
mental problems – 2023: Proceedings of the XIII International Scientific Conference of young scientists, graduates, master and PhD
students. Minsk: ISEU BSU; 2023. p. 201‒202. Russian.
28. Martin P, Shen H, Füllner G, Scholtz G. The first record of the parthenogenetic Marmorkrebs (Decapoda, Astacida, Cambari-
dae) in the wild in Saxony (Germany) raises the question of its actual threat to European freshwater ecosystems. Aquatic Invasions.
2010;5(4):397–403.
29. Lipták В, Mojžičsová M, Gruľa D, Christophoryová J, Jablonski D, Bláha M, Petrusek A, Kouba A. Slovak section of the Danube
has its well-established breeding ground of marbled crayfish Procambarus fallax f. virginalis. Knowledge and Management of Aquatic
Ecosystems. 2017;418:40.
30. Dobrović A, Maguire I, Boban M, Grbin D, Hudina S. Reproduction dynamics of the marbled crayfish Procambarus virginalis
Lyko, 2017 from an anthropogenic lake in northern Croatia. Aquatic Invasions. 2021;16(3):482–498.
31. Seitz R, Vilpoux K, Hopp U, Harzsch S, Maier G. Ontogeny of the Marmorkrebs (marbled crayfish): a parthenogenetic crayfish
with unknown origin and phylogenetic position. Journal of Experimental Zoology. 2005;303a:393–405.
32. Golubev AP, Ulashchik EA, Bodilovskaya OA, Giginyak YUG. Ocenka invazivnogo potenciala partenogeneticheskogo mramor-
nogo raka Procambarus virginalis Lyko, 2017 (Decapoda, Astacidea) v vodoemah umerennoj zony Evropy. Reports of the National
Academy of Science of Belarus. 2024;68(2):129–137. Russian.
33. Veselý L, Buřič M, Kouba A. Hardy exotics species in temperate zone: can «warm water» crayfish invaders establish regardless
of low temperatures? Scientific Reports. 2015;5:16340.
34. Kaldre K, Meženin A, Paaver T, Kawai T. A preliminary study on the tolerance of marble crayfish Procambarus fallax f. virgin-
alis to low temperature in Nordic climate. Marble Crayfish in Nordic. Estonia. 2015;4:54–62.
35. Novitsky RA, Son MO. The first records of Marmorkrebs Procambarus fallax (Hagen, 1870) f. virginalis (Crustacea, Decapoda,
Cambaridae) in Ukraine. Ecologica Montenegriana. 2016;5:44–46.
36. Jimenez SA, Faulkes Z. Establishment and care of a colony of parthenogenetic marbled crayfish, Marmorkrebs. Invertebrate
Rearing. 2010;1(1):10–18.
37. Lewis SD. Biology of Freshwater Crayfish. London; UK; Blackwell Science Ltd; 2002. p. 511–540.
38. Firkins I, Holdich DM. Thermal studies on three species of freshwater crayfish. Freshwater Crayfish. 1993;9(1):241–248.
39. Jonsson A. Life history differences between crayfish Astacus astacus and Pacifastacus leniusculus in embryonic and juvenile
development, laboratory experiences. Freshwater Сrayfish. 1995;8:170–178.
40. Šmietana P, Krzywosz T. Determination of the rate of growth of Pacifastacus leniusculus in Lake Pobłędzie, using polymodal
length-frequency distribution analysis. Bulletin Français de la Pèche et de la Pisciculture. 2006;4;1229–1243.
41. Alekhnovich A, Buřič M. NOBANIS – Invasive Alien Species Fact Sheet – Orconectes limosus [Internet, cited 2024 March 18].
Available from: https://easin.jrc.ec.europa.eu/easin.
42. Ulashchyk KА, Giginjak YuG. The first record of the invasive North American crayfish Faxonius limosus within the water
bodies of Minsk (Belarus). In: Actual environmental problems. XII International scientific conference of young scientists, students,
master students and postgraduates. Minsk: ISEU BSU; 2022. p. 175‒176.
43. Kozák P, Buřič M, Policar T. The fecundity, time of egg development and juvenile production in spiny-cheek crayfish (Orconectes
limosus) under controlled conditions. Bulletin Français de la Pèche et de la Pisciculture. 2006;2;1171–1182.
44. Chucholl С. Population ecology of an alien “warm water” crayfish (Procambarus clarkii) in a new cold habitat. Knowledge and
Management of Aquatic Ecosystems. 2011;401(29):1–21.
45. Fishar MR. Red swamp crayfish (Procambarus clarkii) in River Nile. Egypt: National Institute of Oceanography and Fisheries;
2006. p. 1–34.
46. Luong QT, Shiraishi R, Kawai T, Katsuhara KR, Nakata K. Reproductive biology of the introduced red-swamp crayfish
Procambarus clarkii (Girard, 1852) (Decapoda: Astacidea: Cambaridae) in western Japan. Journal of Crustacean Biology. 2023;43:1–11.
47. Shiyu J, Lisa J, Feng H, Mantang X, Ruojing L, Sovan L, Wei L, Jiashou L, Tanglin Z. Optimizing reproductive performance and
embryonic development of red swamp crayfish Procambarus clarkii by manipulating water temperature. Aquaculture. 2019;510:32‒42.
48. Alekhnovich AV. Rechnye raki Belarusi v sovremennyh usloviyah: rasprostranenie, dinamika chislennosti, produkcionno-
promyslovyj potencial. Minsk: Belarus science; 2016. p. 303. Russian.
49. Bohman P, Degerman E, Edsman L, Sers B. Exponential increase of signal crayfish in running waters in Sweden – due to illegal
introductions? Knowledge and Management of Aquatic Ecosystems. 2011;401:23.
50. Holdich DM, James J, Jackson C, Peay S. The North American signal crayfish, with particular reference to its success as an
invasive species in Great Britain. Ethology Ecology & Evolution. 2014;26(2–3):232–262.
51. Chucholl C, Schrimpf A. The decline of endangered stone crayfish (Austropotamobius torrentium) in southern Germany is related
to the spread of invasive alien species and land-use change. Aquatic Conservation: Marine and Freshwater Ecosystems. 2016;26:44–56.
Статья поступила в редколлегию 12.09.2024.
Received by editorial board 12.09.2024.
ResearchGate has not been able to resolve any citations for this publication.
Article
Full-text available
The red swamp crayfish Procambarus clarkii (Girard, 1852) has been responsible for negative impacts on native benthic fauna and flora in invaded freshwater ecosystems around the world, including Japan. We need to clarify the reproductive biology in the invaded habitats as basic information to effectively control the introduced populations, but the reproductive biology of P. clarkii in Japan (especially in western Japan) has not been well studied. We conducted monthly samplings of P. clarkii from November 2015 to November 2016 in a pond (which does not freeze, even in winter) in Okayama, western Japan, both by using shrimp cage traps and by hand nets to examine aspects of the reproduction, including a form alternation (i.e., Form I and II). We also reared spawning females in the laboratory and calculated the accumulated water temperature during the period to Stage-3 juveniles after spawning. The total number of individuals caught throughout the study period was 6,319 (2,601 males and 2,777 females, with eight of unknown sex and 933 juveniles). The males were all Form I with a breeding status from September to November 2016. We first found ovigerous females in July 2016 and females carrying hatchlings in October 2016, even in January 2016. The form alternation in males was confirmed not only in the cheliped length, but in the hook length. In laboratory observations, approximately 52 days with approximately 1,222 °C degree-days of the accumulated water temperature were necessary to Stage-3 juveniles after spawning. Our results indicate that P. clarkii can reproduce within approximately five months of hatching.
Article
Full-text available
Despite voluminous literature identifying the impacts of invasive species, summaries of monetary costs for some taxonomic groups remain limited. Invasive alien crustaceans often have profound impacts on recipient ecosystems, but there may be great unknowns related to their economic costs. Using the InvaCost database, we quantify and analyse reported costs associated with invasive crustaceans globally across taxonomic, spatial, and temporal descriptors. Specifically, we quantify the costs of prominent aquatic crustaceans — crayfish, crabs, amphipods, and lobsters. Between 2000 and 2020, crayfish caused US120.5millioninreportedcosts;thevastmajority(99 120.5 million in reported costs; the vast majority (99%) being attributed to representatives of Astacidae and Cambaridae. Crayfish-related costs were unevenly distributed across countries, with a strong bias towards European economies (US 116.4 million; mainly due to the signal crayfish in Sweden), followed by costs reported from North America and Asia. The costs were also largely predicted or extrapolated, and thus not based on empirical observations. Despite these limitations, the costs of invasive crayfish have increased considerably over the past two decades, averaging US5.7millionperyear.InvasivecrabshavecausedcostsofUS 5.7 million per year. Invasive crabs have caused costs of US 150.2 million since 1960 and the ratios were again uneven (57% in North America and 42% in Europe). Damage-related costs dominated for both crayfish (80%) and crabs (99%), with management costs lacking or even more under-reported. Reported costs for invasive amphipods (US178.8thousand)andlobsters(US 178.8 thousand) and lobsters (US 44.6 thousand) were considerably lower, suggesting a lack of effort in reporting costs for these groups or effects that are largely non-monetised. Despite the well-known damage caused by invasive crustaceans, we identify data limitations that prevent a full accounting of the economic costs of these invasive groups, while highlighting the increasing costs at several scales based on the available literature. Further cost reports are needed to better assess the true magnitude of monetary costs caused by invasive aquatic crustaceans.
Article
Full-text available
The marbled crayfish (Procambarus virginalis) is a triploid and parthenogenetic freshwater crayfish species that has colonized diverse habitats around the world. Previous studies suggested that the clonal marbled crayfish population descended as recently as 25 years ago from a single specimen of P. fallax, the sexually reproducing parent species. However, the genetic, phylogeographic, and mechanistic origins of the species have remained enigmatic. We have now constructed a new genome assembly for P. virginalis to support a detailed phylogeographic analysis of the diploid parent species, Procambarus fallax. Our results strongly suggest that both parental haplotypes of P. virginalis were inherited from the Everglades subpopulation of P. fallax. Comprehensive whole-genome sequencing also detected triploid specimens in the same subpopulation, which either represent evolutionarily important intermediate genotypes or independent parthenogenetic lineages arising among the sexual parent population. Our findings thus clarify the geographic origin of the marbled crayfish and identify potential mechanisms of parthenogenetic speciation. Gutekunst et al. explore the phylogeographic origins of the marbled crayfish, Procambarus virginalis, a parthenogenetic freshwater species. Based on genomic data of the parent species, they demonstrate that both parental haplotypes of P. virginalis were inherited from the Everglades subpopulation of P. fallax.
Article
Full-text available
Despite the growing number of established populations in Europe, the reproduction dynamics of parthenogenetic marbled crayfish, Procambarus virginalis Lyko, 2017, from populations in the wild is currently understudied. In this study, we performed a systematic seven-month long monitoring of the reproduction dynamics of marbled crayfish population in an anthropogenic lake in continental Croatia. Crayfish were caught monthly by applying the baited stick catch method. We recorded pleopodal fecundity and the number of hatched juveniles in each monthly catch and a random selection of individuals (20 per month) was dissected to determine the ovarian fecundity. Obtained fecundity parameters were correlated with crayfish size (total length, weight and pleon size), body condition (Fulton's condition factor), organosomatic indices (hepatosomatic index: HSI and gonadosomatic index: GSI) and compared with available literature data on marbled crayfish from laboratory-reared or wild populations. Based on the obtained data, we identified two potential reproductive peaks in early summer and mid autumn. However, the continuous presence of individuals with mature ovarian eggs and glair glands throughout almost the entire monitoring period indicates potential reproduction throughout June to November. Ovarian egg number and number of hatched juveniles was significantly correlated with crayfish size and Fulton's condition factor, while GSI exhibited significant variations among analyzed months and was positively correlated with HSI. The number of hatched juveniles in our study was significantly lower compared to literature data for marbled crayfish from populations in the wild and laboratory-reared populations. Collected data offer insights into the understudied reproduction dynamics of marbled crayfish in the wild and represent baseline information for predicting its invasion dynamics and risks of its further spread in this region.
Article
Full-text available
Background The marbled crayfish (Procambarus virginalis) is a monoclonal, parthenogenetically reproducing freshwater crayfish species that has formed multiple stable populations worldwide. Madagascar hosts a particularly large and rapidly expanding colony of marbled crayfish in a unique environment characterized by a very high degree of ecological diversity. Results Here we provide a detailed characterization of five marbled crayfish populations in Madagascar and their habitats. Our data show that the animals can tolerate a wide range of ecological parameters, consistent with their invasive potential. While we detected marbled crayfish in sympatry with endemic crayfish species, we found no evidence for the transmission of the crayfish plague pathogen, a potentially devastating oomycete. Furthermore, our results also suggest that marbled crayfish are active predators of the freshwater snails that function as intermediate hosts for human schistosomiasis. Finally, we document fishing, farming and market sales of marbled crayfish in Madagascar. Conclusions Our results provide a paradigm for the complex network of factors that promotes the invasive spread of marbled crayfish. The commercial value of the animals is likely to result in further anthropogenic distribution. Electronic supplementary material The online version of this article (10.1186/s12898-019-0224-1) contains supplementary material, which is available to authorized users.
Article
Full-text available
The marbled crayfish Procambarus virginalis is a unique freshwater crayfish characterized by very recent speciation and parthenogenetic reproduction. Marbled crayfish also represent an emerging invasive species and have formed wild populations in diverse freshwater habitats. However, our understanding of marbled crayfish biology, evolution and invasive spread has been hampered by the lack of freshwater crayfish genome sequences. We have now established a de novo draft assembly of the marbled crayfish genome. We determined the genome size at approximately 3.5 gigabase pairs and identified >21,000 genes. Further analysis confirmed the close relationship to the genome of the slough crayfish, Procambarus fallax, and also established a triploid AA'B genotype with a high level of heterozygosity. Systematic fieldwork and genotyping demonstrated the rapid expansion of marbled crayfish on Madagascar and established the marbled crayfish as a potent invader of freshwater ecosystems. Furthermore, comparative whole-genome sequencing demonstrated the clonality of the population and their genetic identity with the oldest known stock from the German aquarium trade. Our study closes an important gap in the phylogenetic analysis of animal genomes and uncovers the unique evolutionary history of an emerging invasive species.
Article
Full-text available
Established populations of the non-indigenous parthenogenetically reproducing marbled crayfish Procambarus fallax f. virginalis have been recently reported from various European countries. The colonised sites are usually lentic and relatively isolated from major watercourses and in such cases the immediate threat of the spread of this taxon is limited. Here we report on a marbled crayfish population that is likely to become a seed for colonisation of the Danube in Slovakia. It is located in a channel within the Slovak capital Bratislava in the immediate vicinity of a pumping station that occasionally releases significant amounts of water into the side arm of the Danube. The population is well established with a high growth potential: numerous adult marbled crayfish individuals were observed at the site in September and October 2016 and the progeny (eggs or first two developmental stages) of 27 berried females exceeded 11 000 individuals. The maximum observed fecundity per female reached 647 juveniles in the second developmental stage. The Danube side arm downstream of the pumping station harbours a population of spiny-cheek crayfish Orconectes limosus infected with the crayfish plague pathogen Aphanomyces astaci. We presume that marbled crayfish is already present below the pumping station and it is just a matter of effort and time until it is discovered. The investigated specimens of marbled crayfish were found free of A. astaci, but horizontal transmission from infected spiny-cheek crayfish may be expected, as well as further spread of marbled crayfish in the Danube.
Article
Aquaculture of red swamp crayfish, Procambarus clarkii (Girard, 1852), has developed rapidly worldwide in recent years with promising prospects. However, limited knowledge about temperature effects on reproductive performance and embryonic development has hindered the development of crayfish aquaculture. The two present studies were conducted to identify optimal water temperatures (17 °C, 21 °C, 25 °C, 29 °C and 33 °C) for reproductive performance (experiment 1) and embryonic development (experiment 2) of P. clarkii. Totally, there were 12 replicates, with 480 adults and embryos from 60 ovigerous crayfish selected for experiment 1 and 2, respectively. In the first experiment, the survival of adult crayfish was not significantly affected by the temperatures tested. However, significantly higher feeding rates, spawning rates, and fecundity were obtained at 21 °C and 25 °C when compared to those at 29 °C and 33 °C. Polynomial models and loess regression fitted to the experimental data showed that highest spawning rates and fecundity occurred at 21 °C while shortest duration from mating to spawning was found at 33 °C. In the second experiment, we found that optimal embryonic development was at 25 °C with shorter hatching time and no abnormalities observed. However, while embryos showed abnormalities and subsequently died at 29 °C and 33 °C. We further built a temperature-dependent developmental model for P. clarkii embryos: D (developmental time, days) = 3,140,837(T-2.03)−3.76. Based on these results, the temperature range 21 °C – 25 °C was recommended for adult crayfish reproduction and 25 °C was recommended for embryonic development. This study indicates that manipulating water temperature is an effective alternative to current artificial reproduction techniques (e.g. eyestalk ablation and injection hormones) to induce spawning and embryonic development and thus provides mass production of juvenile P. clarkii for aquaculture.
Article
Marbled crayfish are a globally expanding population of parthenogenetically reproducing freshwater decapods. They are closely related to the sexually reproducing slough crayfish, Procambarus fallax, which is native to the southeastern United States. Previous studies have shown that marbled crayfish are morphologically very similar to P. fallax. However, different fitness traits, reproductive incompatibility and substantial genetic differences suggest that the marbled crayfish should be considered an independent species. This article provides its formal description and scientific name, Procambarus virginalis sp. nov.