Aquacult Int DOI 10.1007/s10499-016-0065-2

Some methodological approaches to the definition of limiting density for aquaculture of freshwater crayfish fingerlings A. P. Golubev1 • A. V. Alekhnovich2 • O. A. Bodilovskaya1 Anilkumar Gopinathan3

•

Received: 4 April 2016 / Accepted: 1 September 2016 Ó Springer International Publishing Switzerland 2016

Abstract The paper defines the methods for maintenance of maximum density (Nmax) in respect of the freshwater crayfish (Astacus leptodactylus) fingerlings (larvae/juveniles), a prospective model organism for aquaculture. The question of optimal maintenance of the fingerlings has been addressed in the present study, considering the following parameters: (1) the ratio between the total area on which the fingerlings are being grown, and the area occupied by one individual, and (2) the planting density dependence on the specific growth rate of differently aged individuals (Cw). Analysis of our results shows that the Nmax values decrease significantly with the growth of individuals (4167, 2222 and 617 ind. m-2 for 30, 65 and 120 days old fingerlings, respectively). The values of Cw for individuals at the age of 30 days, however, do not depend on rearing density within the range of 300–1500 ind. m-2. A linear decrease in Cw is observed in density gradient for older ages. The density at which Cw becomes equal to zero is 3553 ind. m-2 for 65 days old fingerlings, and 1307 ind. m-2 for the 120 days old ones. The revealed differences (with respect to growth rates and planting densities in different age groups) may presumably be caused by the influence of the specific mechanisms of an intra-populational regulation, tenable with the conditions of high densities of fingerlings. Keywords Long-clawed crayfish Astacus leptodactylus  Specific growth rate  Rearing density  Survival  Environment capacity  Aquaculture

& Anilkumar Gopinathan [email protected] A. P. Golubev [email protected] A. V. Alekhnovich [email protected] 1

International Sakharov Environmental Institute of Belarusian State University, Minsk, Belarus

2

Scientific and Practical Centre on Bioresources of National Academy of Sciences of Belarus, Minsk, Belarus

3

School of Biosciences and Technology, VIT University, Vellore, India

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Introduction For the last 150 years, crayfish catches have decreased by 95 % across Europe because of crayfish plague and anthropogenic activities causing drastic changes in crayfish habitats (Skurdal et al. 2002 for review). However, demand for their production remains high because of its market attractiveness. In such circumstances, the most important strategy to meet the increasing demand for crayfish is to enhance their production through aquaculture (Ackefors 2000). This, in turn, requires a significant amount of crayfish juveniles as stocking material. The success of growing crayfish juveniles in aquaculture is defined by many factors: the quality of the aquatic environment (temperature, pH, oxygen regime, water purity, photoperiod and so forth), the quality of the diet, control of disease, the size and age of individuals and the density of their stocking. With our present knowledge, the range of values of the aforementioned abiotic factors and the diet, required for optimization of aquaculture, has been determined with sufficient accuracy (Goessmann et al. 2000; SaezRoyuela et al. 2001; Corkum and Cronin 2004; Ramalho et al. 2008). However, our understanding on the role of stocking density for juvenile cultivation as an important variable, and its dependence on the growth rate of individuals and the level of their mortality, is still enigmatic; it is now being increasingly realized that the information on the interdependence (if any) existing among these variables would be of seminal importance for optimization of aquaculture. The stocking density recommended by different authors varies for several crayfish species ranging between 30 and 2000 individuals m-2 (Ackefors 2000; Ulikowski et al. 2006; Kozak et al. 2007; Harliogˆlu 2009), and some times, as high as 5000 individualsm-2 (Cherkashina 2007). However, most of these recommendations have a rather subjective character and do not have a serious scientific basis. As crayfish are benthic organisms, their juveniles move only in a two-dimensional space. Hence, only a finite number of individuals of the corresponding size can be placed in a limited area. Obviously, this number will constantly decrease in the course of juvenile growth. At this juncture, the following questions remain to be addressed—what is the threshold limit of density that initiates a reduction in growth rate among the stocked fingerlings? Does a threshold limit to the density exist wherein the individuals cease to grow? In other words, what is the optimal density to ensure maximal survival of the crayfish fingerlings? Inasmuch as direct answers to these questions are not available from the existing literature, we, through the results of the present study, offer methods for determining the limiting density for the cultivation of freshwater crayfish fingerlings using the narrowclawed crayfish Astacus leptodactylus (Eschscholtz 1823) as the model. The first method is based on the assessment of the conjugated changes of the area occupied by a growing individual and a relation between it and a total area on which cultivation is carried out. The second method involves the analysis of changes in the specific growth rate of uneven-aged individuals in a stocking density gradient.

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Materials and methods Determination of the area occupied by freshwater crayfishes It seems that the top limit of stocking density at which the freshwater crayfish juveniles lose their ability to grow can be defined based on the surface area occupied by one individual (S). An A. leptodactylus juvenile has 4 pairs of walking legs standing out from the sides of a cephalothorax and pair of long claws directed forward (Fig. 1A). Therefore the shape of the surface area occupied by one individual is close to the shape of an ellipse (Fig. 1B). Its longitudinal axis (AB) corresponds to the maximum length of an individual (ML), i.e., the distance from the claw tip to the end of telson. The width (CD) corresponds to the largest width of an individual (MW), i.e., to the magnitude of the fourth (back) pair of walking legs (Fig. 1B). Hence, the area occupied by one individual of A. leptodactylus can be determined according to: p ð1Þ S ¼ MW ML 4 We determined the values of ML and MW in samples of A. leptodactylus fingerlings at 30 days (the period of early development corresponding to the first 1–2 intermolt periods in newborn larvae), 65 days (juveniles that have fully undergone metamorphosis) and 120 days old (the duration of a vegetation season for fingerlings in the reservoirs of the temperate zone). The calculations of the specific growth rate of individuals were carried out based on the available literature, by data analysis of the weight or linear growth of A. leptodactylus fingerlings depending on stocking density in experimental conditions. We analyzed data only on the growth of A. leptodactylus fingerlings in laboratory aquaria or equivalent conditions (Grozev and Zaikov 2000; Ulikowski and Krzywosz 2004, 2006; Ulikowski et al. 2006; Mazlum 2007; Harliogˆlu 2009). The A. leptodactylus newborns used in the present investigation were brought to the laboratory from egg-bearing females collected from natural water bodies or aquaculture facilities. Fingerlings of the same age, grown in similar temperature and other environmental conditions, were taken for comparison (Cherkashina 2007; Grozev and Zaikov 2000; Harliogˆlu 2009; Mazlum 2007; Ulikowski and Krzywosz 2004, 2006; Ulikowski et al. 2006). The extrinsic parameters such as temperature, oxygen content and pH, were ranging to the tune of 22–25 °C, 5 to 7 ml O2l-1 and 8.0–8.3, respectively, so as to suit to the optimal conditions for A. leptodactylus juveniles. Individuals were fed ad libitum on commercial diets (crude protein 50–62 %, fat 5–11 %, minerals up to 11 %, fiber

Fig. 1 A Appearance of an Astacus leptodactylus fingerling at the age of 1.5 months. B A. leptodactylus body shape inscribed in an oval. C Location of A. leptodactylus fingerlings on a plane according to the principle of ‘‘bee honeycombs’’. Explanations are in the text

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1–1.5 %). Recycling of water through biofilters or its periodic changing provided an acceptable quality of the medium for culture. The specific growth rate values based on weight of individuals (Cw, day-1) were calculated by a conventional method (Alimov 1989): Cw ¼

ln Wt  ln Wo ; t  to

ð2Þ

where Wt is the average weight of individuals (mg) at the age of t (days), and Wo is the average weight of newborn larvae (mg) for which to = 0. In the calculations of Cw, the average weight of newborn larvae was taken from the available literature sources. If such data were not available, the value of Wo was taken equal to 32 mg. If data only on the linear growth of fingerlings were presented in relevant publications, the calculations of Cw were performed as follows: The values of Cw are in a simple ratio with the specific rate of their linear growth (CL), which is calculated by the same way (2): Cw ¼ bCL ;

ð3Þ

where ‘‘b’’ is the indicator of a power in the equation of the body weight (W) dependence of the body length (L) of an individual. W ¼ aLb

ð4Þ

In Eq. (4), for a large number of the species of aquatic invertebrates, the value of ‘‘b’’ is usually in the range of 2.5–3.5 (Alimov 1989). However, since in most of the works, which we used, Eq. (4) for A. leptodactylus juveniles is not given for calculations (3), we assumed that b = 3.0. In the majority of publications used, only the densities of fingerlings at the beginning (N1) and end (N2) of the growing period are given. However, using the arithmetic mean for values of average density for rearing period, Na ¼

N1 þ N2 2

ð5Þ

assumes a linear reduction in the density of individuals with their age, which seems to be wrong. We previously have shown (Kulesh and Alekhnovich 2010) that the mortality of A. leptodactylus fingerlings is maximal during the first month of their life (including the first 1–2 intermolt periods) at their cultivation in the conditions of high density; however, mortality significantly decreases at the older ages (2–4 months) (Fig. 2). In general, an age-related decrease in the stocking density of A. leptodactylus fingerlings during the first 3–4 months of their life can be approximated by not a linear, but a negative power function: Ns ¼ N1 ta ;

ð6Þ

where Ns is the rearing density of fingerlings at the age of t (days), N1 is their density at the age of 1 day, a is an empirical constant. The initial stages of the life cycle of almost all species of aquatic invertebrates are characterized by high mortality, which gradually decreases with age (Begon et al. 1996). Therefore, it is quite probable that the revealed dependence (6) is typical not only for A. leptodactylus fingerlings but for other species of freshwater crayfish as well. Hence, the practice of using the arithmetic mean values of the density of individuals (5) at cultivation could lead to a significant overstatement of density for the older-aged

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Aquacult Int Fig. 2 Decrease in the density of Astacus leptodactylus fingerlings with age at keeping in trays. 1 Initial density of 300 ind. m-2. 2 Initial density of 200 ind. m-2. Accordingly (Kulesh and Alekhnovich 2010)

fingerlings when its inhibitory effect on the growth rate of individuals is expressed most strongly. Based on Eq. (6), it would be more reasonable to use the geometric mean values (Ng) of the initial (N1) and the final (N2) densities for calculating the average density of fingerlings during the entire cultivation period, as shown below: Ng ¼ ðN1  N2 Þ0:5 :

ð7Þ

The calculated regression equations between Cw and Ng were verified on presence/ absence of heteroscedasticity by White test. All the calculations were performed using the software packages ‘‘Statistica 8.0’’ and ‘‘EViews 7.’’

Results From our previous studies with the samples of A. leptodactylus fingerlings from the water reservoirs of Belarus, the average length–width relation has been computed as MW = 0.75ML. Based on this, we have estimated the values of the area occupied by one individual (cm2), and subsequently for individuals aged 30, 65 and 120 days (Table 1). Further, on the basis of the S values, the maximum possible stocking density (Nmax) of individuals in the respective age groups has been calculated by equation: Nmax ¼

1 m2 S

ð8Þ

where S values are expressed in m2. Table 1 Linear sizes of individuals, the area square occupied by them (S) and the maximum planting density (Nmax) of Astacus leptodactylus fingerlings at different ages Nmax, indm-2, calculated accordingly (8)

Ncr indm-2, calculated accordingly (12)

2.4 9 10-4

4167

–

2.08

4.5 9 10-4

2222

3553

3.78

15.0 9 10-4

667

1307

Age, days

ML, cm

MW, cm

30

2.02

1.52

65

2.77

120

5.04

S, m2; calculated accordingly (1)

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Obviously, to a certain extent, the values of Nmax can be considered as a maximum medium capacity during the cultivation of A. leptodactylus fingerlings in an aquaculture in optimal medium conditions and the absence of feed limitation. In the process of the growth of fingerlings, the S values quickly increase with age, and accordingly, the Nmax values decrease (see Table 1). The data on the stocking density (N, ind. m-2) dependence on the specific growth rate (CW, day-1) of A. leptodactylus fingerlings in different age groups are shown in Fig. 2. Each Cw data presented here were calculated on W values for not less than 20 individuals. Variability of W values for all the sets of experiments was rather low—the coefficients of variations for W did not exceed 22 % even at maximal densities (Mazlum 2007). It is thus revealed that there exists no statistically significant N dependence of CW (correlation coefficient r being -0.120) in the case of fingerlings at the age of 30 days (Fig. 2). This can be explained by the initial stocking density of A. leptodactylus newborn larvae did not exceed 1500 ind. m-2 in the studies examined. It is significantly lower than the calculated Nmax of the 30 days old fingerlings, which was 4167 ind. m-1 (Table 1). For the other two age groups (65 and 120 days), a clear Cw reduction with increasing stocking density was found (Fig. 2). The revealed dependence can be described by a linear regression equation of the type: Cw ¼ ab  N;

ð9Þ

where ‘‘a’’ is the maximum Cw value achieved at planting density (N) close to zero, and ‘‘b’’ is an empirical constant characterizing an inclination slope of a regression line to the X-axis. In a numerical form, Eq. (9) for the 65 days old fingerlings could be: Cw ¼ 0:03340:0000094  N;

ð10Þ

Our analysis revealed the existence of a statistically significant negative correlation between Cw and N for (10) (r = -0.871; p = 0.024). For the age of 120 days, which corresponds approximately to the duration of the vegetative period of growth for fingerlings, the following equation applies: Cw ¼ 0:03530:000027  N;

ð11Þ

Here again, there exists a statically significant negative correlation between Cw and N (r = -0.999; p = 0.017). The White test rejected the heteroscedasticity occurrence for Eqs. (10) and (11) as for the data presented at Fig. 1A (p [ 0.1). Thus, it becomes obvious that the Cw values of 65 and 120 days old fingerlings would be reduced in direct proportion to the stocking density. Significantly, the Cw reduction with increasing stocking density is expressed more strongly in older individuals than in younger ones (Fig. 2). Eq. (9) allows us to determine the theoretical rearing density (Ncr) at which the growth of individuals stops, i.e., when the value of Cw becomes almost equal to zero. Since Ncr ¼ a=b;

ð12Þ

then the values for the 65 days old fingerlings, Ncr = 0.033342/0.0000094 = 3553 ind. m-2, and those for the 120 days old, Ncr = 0.035264/0.000027 = 1307 ind.m-2. The obtained Ncr values for the specified ages are almost twice as large as that for the Nmax values calculated on the area occupied by one individual (Table 1). One of the reasons for such discrepancies is probably a certain inflation of the area occupied by one

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individual. Theoretically, a possible location of individuals on a plane according to the principle of ‘‘bee honeycombs’’ increases their number per unit area (Fig. 1C). The other possible reasons are the absence of the direct data on the temporal dynamics of mortality during experiments in the majority of used publications (see above in ‘‘Materials and methods’’ section) and underestimation of fine mechanism of intrapopulation density regulation.

Discussion On the basis of the data given above, it becomes very obvious that the Cw values of A. leptodactylus fingerlings at the ages of 65 and 120 days are reduced in direct proportion to the increase in rearing density; the extent of Cw reduction (with the increase in stocking density) is expressed more strongly in older individuals than in younger ones (Fig. 3B). As calculated by both the methods, the maximum values of the rearing density of A. leptodactylus fingerlings at the ages of 65 and 120 days in aquaculture conditions showed rather high convergence (Table 1). This gives sufficient grounds to believe that

A 0,080

Cw, days-1

0,070 0,060 0,050 0,040 0,030 100

200

300

400

500

600

700

800

900

Geometric mean of density, ind.•m-2

B

0,035 0,034 0,033

Cw, day-1

Fig. 3 Dependences between densities of Astacus leptodactylus fingerlings (ind. m-2) at rearing and their specific growth rate (Cw, day-1). A Age of 30 days; accordingly (Cherkashina 2007; Grozev and Zaikov 2000; Ulikowski and Krzywosz 2004; Ulikowski et al. 2006). B Ages of 65 days (1) and 120 days (2); accordingly Harliogˆlu (2009) and Mazlum (2007), respectively. Straight 1 is the regression line of Eq. (10); Straight 2 is the regression line of Eq. (11). Dotted curves—95 % confidence level

0,032 0,031 0,030 0,029

1

0,028 0,027 0

100

200

2

300

400

500

600

Geometric mean of density, ind.•m -2

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medium capacity for the cultivation of fingerlings will consistently decline as they grow; by the age of 120 days, the rearing density will not exceed 600–1200 ind. m-2. A negative relationship between the rearing density of fingerlings at the older ages and the specific rate of growth at these ages (Fig. 2) is apparently caused by the rapid exhaustion of medium capacity in the process of the growth of individuals. The present study thus helps us to opt between the alternative situations such as the larger quantity of small individuals or the smaller quantity of larger individuals per unit area during the growing period. The correlation between the growth rate and the rearing density does not seem to be applicable for the individuals of 30 days old, as the medium capacity for this age group is far from its limit even at a sufficiently high density (up to 1600 ind. m-2) (see Table 1). Previous experiments reveal that in the A. leptodactylus fingerlings of 30–32 days old, the high survival and growth rate are rather independent of the density (Franke et al. 2013). Obviously, the growth rate of the fingerlings of this species at a minimal stocking density could primarily be determined by other factors—temperature, diet and so forth. Under increased stocking density, the growth of individuals could lead to gradual exhaustion of the vital space resources for them, which is a powerful limiting factor. Therefore, under the conditions of constant density, the growth of individuals may stop as they attain a certain size. This theoretical conclusion could be substantiated through the socalled ‘‘battery culture’’ experiments wherein each of the crayfish juveniles would be maintained in separate cells (Barki et al. 2006). This method allows resolving a number of negative effects of increasing density, including intraspecific competition, postmolt cannibalism and so forth. However, a constant increase in the cell area paralleled with the process of the growth of individuals may not always expedient from the economic standpoints. Therefore, crayfish breeding in most cases of aquacultural practices is being performed involving groups of candidates wherein accounting density effect on the growth and survival of individuals becomes imperative. In crayfish aquaculture, the stocking density is considered a complex factor; its influence on the growth of individuals is realized both directly and indirectly through the dynamics of survival. A direct impact may be realized through deterioration in water quality due to metabolite accumulation and feed residues, the shortage of food and shelters, greater intraspecific competition and postmolt cannibalism (Barki et al. 2006); changing the social population structure, behavior peculiarities, and chemical and visual signals (Lowery 1988) could add to the negative impacts that could restrain growth. Numerous studies on hydrobionts from different taxons (such as shrimps, mollusks, fish and amphibian larvae) have shown that a decrease in the growth of individuals (and hence, their average size), an increase in their mortality and a dimensional differentiation are seen coupled with increase in rearing density (Schwartz et al. 1976; Golubev 1999; Huner 1999; Barki and Karplus 2004). Two size-related groups of A. leptodactylus fingerlings are clearly distinguished in the conditions of an aquaculture at an initial density of 2000 ind. m-2, at the age of 3 months (Golubev et al. 2015). The first group, smaller in number (accounting for 3 % of the total population) encompassed the largest individuals (referred to as ‘‘leaders’’) with a body length of 30–36 mm. The second group (approximately 97 % of the total population) comprised far smaller individuals (‘‘outsiders’’) of the size of 17–30 mm. This affords a typical example of the formation of social structure in the given population, with the domination of the ‘‘leaders’’ over others (‘‘outsiders’’). It is suggested that a specific effect of leader metabolites accumulated in a limited volume of water is instrumental in the

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growth inhibition of ‘‘outsiders’’ (Schwartz et al. 1976). Therefore, ‘‘leaders’’ attain success in the intraspecific competition for food and spatial resources with outsiders, which in turn can perspectively provide a faster growth of this small group under the conditions of increased density. Freshwater crayfish essentially differs from other candidates of aquaculture such as mollusks or non-predatory fishes, as they have strikingly different forms of aggressive behavior and cannibalism (Taugbøl and Skurdal 1992). Postmolt cannibalism could lead to a substantial decrease in the number of crayfish juveniles. Postmolt individuals are the most vulnerable cohort, being challenged with the threat of cannibalism. In the first summer of life, A. leptodactylus juveniles molt no less than 5–6 times. As molting juveniles occur asynchronously, the molted individuals become potential targets for attack from the numerous individuals that are at the stage of intermolt. As crayfish molts occur more often during daytime, the provision for a sufficient number of suitable shelters, wherein crayfish as twilight animals could hide during the daytime, and properly selected lighting mode, could significantly reduce postmolt cannibalism (Franke et al. 2013). Another important condition for the successful cultivation of crayfish is on account of their behavioral characteristics. An increase in crayfish stocking density could lead to the intensification of intraspecific competition, which manifests in particular in increasing the number of collisions among themselves, leading to aggressive behavior. This in turn, may reduce crayfish growth rate due to the growing energy expenditures. Interestingly, among the groups of A. leptodactylus juveniles grown in aquaria, the duration and intensity of antagonistic clashes were shown to increase initially, but to decline as the growth of individual proceeds and the formation of a hierarchical structure ensues (Goessmann et al. 2000). At that juncture, as the social circumstances changed, the crayfish population was seen to evade from the strategy of a struggle against other individuals. Interestingly, an increase in the size of a group reduces the number of fights by 50 % and their duration by 80 % (Patullo et al. 2009). The aggressive behavior could also lead to a decrease in food consumption, as the crayfish spent more time in fighting with each other. With an increase in the heterogeneity of the habitat (growth in the number of potential hiding places and shelters), the rate of food consumption (if in abundance) enhances, inasmuch as reduction in intraspecific competition could lead to availability of more time on food search and consumption (Corkum and Cronin 2004). In experiments with the red swamp crayfish Procambarus clarkii, it was shown that an increase in the crayfish density if coupled with an increase in the number of shelters can reduce the negative impact on the growth rate of individuals due to the shifting of an active aggressive behavior toward a passive behavior (Ramalho et al. 2008). Further, the absence of a statistically significant dependence between the density of the species and their survival of a less aggressive Australian redclaw crayfish Cherax quadricarinatus (Jones and Ruscoe 2000) supports this contention. It may also be suggested that the reduction of energy costs for aggressive interactions among individuals can lead to an increase in their growth rate. Besides, the specific growth rate of C. quadricarinatus juveniles as well as A. leptodactylus (Fig. 2) decreased with increasing their density in experiment (Jones and Ruscoe 2000).

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Conclusion To conclude, the previous attempts to find the key factors regulating the growth rate of crayfish juveniles in the context of aquaculture, have not given unambiguous results. Obviously, the optimum survival depends on a complex interaction involving stocking density, food provision, environment heterogeneity, intraspecific competition, and the behavior of individuals. The present study unequivocally defines the dependence existing among the important variables such as stocking density (involving the total space available for aquaculture and the space occupied by the individuals) and growth rate of differently aged classes of the fingerlings of A. leptodactylus. This could be considered the first ever report establishing such a relation defining the dependence of growth rate on limiting density in an age-dependent manner. In light of the present study, the obtained results could arguably be applied for other species of crayfishes as well. This, in turn, could create a basis for further development of an optimal strategy for their cultivation (with a view to obtain maximum output of the individuals of desirable sizes and weight), which also could be instrumental in largely eliminating the negative consequences of various factors (cannibalism, and intraspecific competition, for instance). Further, inasmuch as the relative impact of planting density on growth rate and optimal survival of the individuals in question may vary with different species, further research using appropriate schemes of experimental design and methods of a multiple-factor statistical analysis would also become very much imperative. Acknowledgments These studies were performed in the framework of the International Scientific Project entitled ‘‘Ecological and biochemical aspects of the regulation of growth and reproduction in decapod crustaceans and anostracans for the revelation of their potentials in an aquaculture’’ (DST/INT/BLR/P-6/ 2014 dated 15 April 2015) carried out by the International Sakharov Environmental Institute of the Belarusian State University (Minsk, Belarus) and the School of Biosciences and Technology, VIT University (Vellore, India). The project is funded by the State Committee on Science and Technologies of the Republic of Belarus and the Department of Science and Technology, Government of India.

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