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Animal performance and welfare of giant freshwater prawn (Macrobrachium rosenbergii) subjected to feed restriction

ABSTRACT

Behavior activities of giant freshwater prawn Macrobrachium rosenbergii juvenile, their performance, and acquired lesions when under temporary feed restrictions were analyzed. Five animals/experimental units (10 prawns/m2) were employed for treatments DFL – daily feed supply in the light phase; DFD – daily feed supply in the dark phase; AFL – alternating feed supply in the light phase; and AFD – alternating feed supply in the dark phase, for a 24-hour period, with four replications each. Prawns were fed a pellet diet, twice a day, with 10% of their biomass/day. Specimens were monitored during 60 consecutive days, with behavior recording daily and weighed every 10 days, with assessment of lesions and/or amputated limbs at the end of the experimental period. Types of behavior comprised exploring, grooming, inactivity, crawling, swimming, excavation, burrowing, agonism, and feed ingestion by scan sampling, with instantaneous registration every 60 s, in 15-min windows, before and after feed, in light and dark phases. Feed restricted in alternate days during light and dark phases did not interfere in growth or survival of the specimens, with increase in apparent feed intake and less feed conversion ratio and specific growth rate. Agonistic behavior was higher in specimens with feed restrictions, with an increase in the number of lesions and amputations. The above demonstrates welfare decrease in farmed M. rosenbergii and depreciation in the quality of the final product.

Keywords:
applied ethology; Malaysian giant prawn; prawn culture

1. Introduction

Different aquatic animal species are farmed to attend food demand worldwide. Crustaceans have been highlighted due to high market price and to their ability to adapt to several culture conditions (FAO, 2018FAO - Food and Agriculture Organization of the United Nations. 2018. The State of World Fisheries and Aquaculture: Meeting the Sustainable Development Goals. Food and Agriculture Organization of the United Nations, Rome.). Freshwater prawns have stood out among crustaceans. In fact, they are farmed in several countries, with world production reaching 216,857 tons, worth 1.33 billion US dollars, in 2014 (FAO, 2016FAO - Food and Agriculture Organization of the United Nations. 2016. FAO yearbook. Fishery and Aquaculture Statistics 2014. Food and Agriculture Organization of the United Nations, Rome.). Giant freshwater prawn, Macrobrachium rosenbergii, is the most important cultivable freshwater prawn species due to fairly high growth rates, wide temperature range (15-35 °C) and salinity tolerance (Mukhopadhyay et al., 2003Mukhopadhyay, P. K.; Rangacharyulu, P. V.; Mitra, G. and Jana, B. B. 2003. Applied nutrition in freshwater prawn, Macrobrachium rosenbergii, culture. Journal of Applied Aquaculture 13:317-340. https://doi.org/10.1300/J028v13n03_06
https://doi.org/10.1300/J028v13n03_06...
).

Feed conversion ratio and cost-benefit in feeding management are, as a rule, the most significant fraction, with up to 50% of production costs, whilst feed management is a crucial factor to calculate the viability of a prawn farm (Akyiama and Polanco, 1997Akyiama, D. and Polanco, B. 1997. Semi-intensive shrimp farm management: Technical manual. Polanco, B., ed. American Soybean Association, Caracas.; Arnold et al., 2016Arnold, S.; Smullen, R.; Briggs, M.; West, M. and Glencross, B. 2016. The combined effect of feed frequency and ration size of diets with and without microbial biomass on the growth and feed conversion of juvenile Penaeus monodon. Aquaculture Nutrition 22:1340-1347. https://doi.org/10.1111/anu.12338
https://doi.org/10.1111/anu.12338...
). Feed-restriction strategy in aquaculture is a stressful technique, even though it has been widely employed as a strategy to guarantee less feed expenditure and low labor costs (Maciel et al., 2018Maciel, J. C.; Francisco, C. J. and Miranda-Filho, K. C. 2018. Compensatory growth and feed restriction in marine shrimp production, with emphasis on biofloc technology. Aquaculture International 26:203-212. https://doi.org/10.1007/s10499-017-0209-z
https://doi.org/10.1007/s10499-017-0209-...
). Cyclic feed restriction may be a useful strategy to minimize negative environmental changes triggered by feed excess in ponds (Mohanty and Mohapatra, 2017Mohanty, R. K. and Mohapatra, A. 2017. Cyclic feed restriction on growth compensation of Penaeus monodon (Fabricius): science meets practice. Indian Journal of Geo-Marine Sciences 46:2008-2016.).

In spite of the social and behavioral complexity in populations, studies in applied ethology to develop new management practices are scarce. Li et al. (2008)Li, Z.; Xie, S.; Wang, J. and Chen, D. 2008. Compensatory growth in shrimp Macrobrachium nipponense following starvation. Sichuan Journal of Zoology 27:335-339. reported compensatory growth of M. nipponense during feed deprivation. Marques and Lombardi (2011)Marques, H. L. A. and Lombardi, J. V. 2011. Compensatory growth of Malaysian prawns reared at high densities during the nursery phase. Revista Brasileira de Zootecnia 40:701-707. https://doi.org/10.1590/S1516-35982011000400001
https://doi.org/10.1590/S1516-3598201100...
verified the occurrence of compensatory growth in M. rosenbergii stocked in cages, under high densities, during the nursery phase, and suggested partial compensatory growth in this phase. Addicionally, Rahman et al. (2019)Rahman, F.; Ghosh, A. K. and Islam, S. S. 2019. Effect of time-restricted feeding and refeeding regimes on compensatory growth, body composition, and feed utilization in prawn (Macrobrachium rosenbergii) culture system. Journal of Applied Aquaculture 1-14. https://doi.org/10.1080/10454438.2019.1661328
https://doi.org/10.1080/10454438.2019.16...
stated that time restriction could be applied in M. rosenbergii culture without detrimental effects on growth, feed efficiency, and nutrient utilization.

Research in applied ethology mainly aims at analyzing and enhancing the welfare of farmed animals. It is a concern of the contemporary society that founded the International Society for Applied Ethology (Huntingford et al., 2012Huntingford, F.; Jobling, M. and Kadri, S. 2012. Aquaculture and behavior. Blackwell Publishing, Oxford.). Since research on animal performance and its relationship with feeding and welfare of M. rosenbergii are scarce, it is relevant to assess the behavioral activities and lesions suffered by these animals when subjected to temporary feeding restrictions.

2. Material and Methods

Juvenile specimens of giant freshwater prawn were retrieved from the municipality of Macaíba, state of Rio Grande do Norte, Brazil (5.885552 S; 35.365886 W), and conditioned in two 80-L plastic boxes, with constant aeration, at 27.2 °C and 0.5 g/L salinity. They were then transferred to Natal, RN, Brazil (5.841720 S; 35.202411 W).

Prawns were weighed on a scale (2.25±0.53 g, n = 20) in the laboratory, conditioned, and acclimated in experimental units. During acclimatization, the feeding management of animals under experimental conditions was considered. Eight 250-L (100 × 50 × 50 cm) aquariums were employed for each treatment, with fine sandy substrate, and maintained within a closed water circulation system, with artificial light, constant aeration, and continuous filtration with biochemical and biological Canister filters. Five animals/aquarium were established at a stocking density of 10 prawns/m2, following pattern used by producers (5-10 prawns/m2 for mixed populations). Four artificial havens (PVC tubes) were placed in each aquarium. For animal behavior and performance under periodic feed restriction to be analyzed, M. rosenbergii underwent the following treatments, with four replications: DFL – daily feed supply in the light phase; DFD – daily feed supply in the dark phase; AFL – alternating feed supply in the light phase; and AFD – alternating feed supply in the dark phase, for a 24-h period.

The laboratory comprised two rooms with artificial lights. Photoperiod was controlled by a 12:12 h light/dark cycle timer. In one room, the light phase occurred from 06:00 to 18:00 h, whilst the dark phase occurred from 18:00 to 06:00 h (natural photoperiod); the photoperiod in the other rooms was inverted. Consequently, the four experimental units in the light phase and the four experimental units in the dark phase could be monitored at the same time. Aquariums were illuminated with 32-W white fluorescent lamps for the light phase and with 15-W red incandescent lamps for the dark phase. This type of lighting was used due to the prawn's lack of reaction to it (Pontes and Arruda, 2005Pontes, C. S. and Arruda, M. F. 2005. Comportamento de Litopenaeus vannamei (Boone) (Crustacea, Decapoda, Penaeidae) em função da oferta do alimento artificial nas fases claras e escuras do período de 24 horas. Revista Brasileira de Zoologia 22:648-652. https://doi.org/10.1590/S0101-81752005000300019
https://doi.org/10.1590/S0101-8175200500...
).

Prawns were individually weighed on a digital balance every ten days (T0, T10, T20, and T30) to monitor growth. Animals were observed in each treatment during 30 consecutive days to record the species' behavior. They were given pellet feed, throughout the experiment, at 10% of their biomass/day from troughs (transparent acrylic trays), with 35% crude protein, twice a day, at 08:00 and 16:00 h, complying with the treatment applied.

Reports on behavior of prawns started after 10 days of adaptation to the physical conditions of the aquaria (Sick et al., 1973Sick, L. V.; White, D. and Baptist, G. 1973. The effect of duration of feeding, amount of food, light intensity, and animal size on rate of ingestion of pelleted food by juvenile penaeid shrimp. The Progressive Fish-Culturist 35:22-26. https://doi.org/10.1577/1548-8659(1973)35[22:TEODOF]2.0.CO;2
https://doi.org/10.1577/1548-8659(1973)3...
; Pontes et al., 2006Pontes, C. S.; Arruda, M. F.; Menezes, A. A. L. and Lima, P. P. 2006. Daily activity pattern of the marine shrimp Litopenaeus vannamei (Boone 1931) juveniles under laboratory conditions. Aquaculture Research 37:1001-1006. https://doi.org/10.1111/j.1365-2109.2006.01519.x
https://doi.org/10.1111/j.1365-2109.2006...
) and after the establishment of social hierarchy (Fero et al., 2007Fero, K.; Simon, J. L.; Jourdie, V. and Moore, P. A. 2007. Consequences of social dominance on crayfish resource use. Behaviour 144:61-82. https://doi.org/10.1163/156853907779947418
https://doi.org/10.1163/1568539077799474...
). Types of behavior registered every day in each treatment comprised exploration, grooming, inactivity, crawling, swimming, excavation, burrowing, and agonism (Santos and Pontes, 2016Santos, D. B. and Pontes, C. S. 2016. Behavioral repertoire of the giant freshwater prawn Macrobrachium rosenbergii (De Man, 1879) in laboratory. Journal of Animal Behaviour and Biometeorology 4:109-115. https://doi.org/10.14269/2318-1265/jabb.v4n4p109-115
https://doi.org/10.14269/2318-1265/jabb....
). Registration method consisted of scan sampling (Martin and Bateson, 2007Martin, P. and Bateson, P. 2007. Measuring behaviour: an introductory guide. 3rd ed. Cambridge University, Cambridge.; Yamamoto and Volpato, 2011Yamamoto, M. E. and Volpato, G. L. 2011. Comportamento animal. EdUFRN, Natal.), applied in windows, 15 min before and 15 min after feed for each experimental unit twice a day (light and dark phases) per treatment, with instantaneous reports every 60 s, during 30 consecutive days for daily feed, with a further 30 days for alternating feed treatments, totaling 60 days and 320 h of observation. Timetables for windows lay between 08:00 and 09:00 h and between 20:00 and 21:00 h – when two aquariums were observed during the light phase and two during the dark phase, between 16:00 and 17:00 h, and between 04:00 and 05:00 h. Reports had to be undertaken by two observers at the same time. Observers underwent a trustworthy test with 95% confidence for data observation. At the end of the experiment, biometry was performed, and lesions or amputated body structures, an indication of fighting incidents characteristics of agonistic behavior, were detected to evaluate the relationship between feed restriction and animal welfare.

The water quality of the aquaria was monitored daily. Water salinity was kept at 0 g/L (portable refractometer); pH at 7.85±0.2 (pH meter); water temperature at 27.5±1 °C (electrode thermometer); ammonia at 0.02±0.06 mg/L, and dissolved oxygen above 5 mg/L (Instrutherm digital oximeter). Water quality remained constant throughout the observation period, at the ideal standard for the culture of the species (Valenti, 1998Valenti, W. C. 1998. Carcinicultura de água doce: tecnologia para produção de camarões. Fapesp/Ibama, Brasília.).

Feed intake, or rather, the difference between the quantity provided (dry weight) and the surplus in the trough (removed 2 h after placed in the water) was evaluated daily during the experiment. At the end of the experiment, surplus of each treatment was added so that the apparent intake of prawns could be calculated. Feed efficiency (FE) was determined by intake rates (Kureshy and Davis, 2002Kureshy, N. and Davis, D. A. 2002. Protein requirement for maintenance and maximum weight gain for the Pacific white shrimp, Litopenaeus vannamei. Aquaculture 204:125-143. https://doi.org/10.1016/S0044-8486(01)00649-4
https://doi.org/10.1016/S0044-8486(01)00...
):

I n g e s t i o n ( a p p a r e n t c o n s u m p t i o n ) = f e e d p r o v i d e d s u r p l u s F e e d e f f i c i e n c y = f i n a l w e i g h t i n i t i a l w e i g h t f e e d c o n s u m p t i o n

Weight gain was calculated at the end of the experiment with a two decimal digit precision scale. Weight gain, retrieved from rates obtained (Kureshy and Davis, 2002Kureshy, N. and Davis, D. A. 2002. Protein requirement for maintenance and maximum weight gain for the Pacific white shrimp, Litopenaeus vannamei. Aquaculture 204:125-143. https://doi.org/10.1016/S0044-8486(01)00649-4
https://doi.org/10.1016/S0044-8486(01)00...
), determined specific growth rate (SGR) (Wu and Dong, 2002Wu, L. and Dong, S. 2002. Effects of protein restriction with subsequent realimentation on growth performance of juvenile Chinese shrimp (Fenneropenaeus chinensis). Aquaculture 210:343-358. https://doi.org/10.1016/s0044-8486(01)00860-2
https://doi.org/10.1016/s0044-8486(01)00...
):

W e i g h t g a i n ( g ) = f i n a l w e i g h t i n i t i a l w e i g h t S G R ( % . d a y 1 ) = L n f i n a l w e i g h t L n i n i t i a l w e i g h t n u m b e r o f d a y s × 100

Dead specimens were counted every day, in the morning, to calculate the final survival rate (SR), defined by Bautista-Teruel et al. (2003)Bautista-Teruel, M. N.; Eusebio, P. S. and Welsh, T. P. 2003. Utilization of feed pea, Pisum sativum, meal as a protein source in pratical diets for juvenile tiger shrimp, Penaeus monodon. Aquaculture 225:121-131. https://doi.org/10.1016/S0044-8486(03)00284-9
https://doi.org/10.1016/S0044-8486(03)00...
:

S R ( % ) = f i n a l n u m b e r o f p r a w n s i n i t i a l n u m b e r o f p r a w n s × 100

Statistical Analyses were performed with SIGMAPLOT 10.0 (2006). Depending on premises required for data parametricity (Normality – Kolmogorov-Smirnov; Homoscedasticity – Shapiro-Wilks) (Zar, 1999Zar, J. H. 1999. Bioestatistical analysis. 4th ed. Prentice-Hall, New Jersey.), results were analyzed with ANOVA or Kruskal-Wallis test. For significant differences, we applied the post hoc Tukey's test. A significance level of 5% was used to assess the results. Lesions or amputated body structures were represented through descriptive statistics, and SR was reported in the text.

Behavioral variables (exploring, grooming, inactivity, crawling, swimming, excavation, burrowing, agonism, and feed intake) were analyzed according to the model below, in which N is the total sample size, ni is the size in each treatment, and Ri is the sum of the ranks of each treatment of dependent variable:

H = 12 N ( N + 1 ) × i = 1 k R i 2 n i 3 ( N + 1 )

Animal performance (weight, apparent intake, FE, and FCR) were analyzed with one-way ANOVA, according to the following model, in which K is the treatment number, N is the sample size, nk is the amount of individuals per treatment, x¯k is the mean of dependent variable in a treatment, x¯total is the mean of dependent variable in all treatments, xik is the value of na individual of a treatment, K – 1 is the degree of freedom of the model, and NK is the degree of freedom of the residue:

F = ( n k ( x ¯ k x ¯ t o t a l ) 2 K 1 ) ( ( x i k x ¯ k ) 2 N K )

Then, in the post hoc Tukey's test, we followed the model:

H S D = x ¯ 1 x ¯ 2 ( ( x i k x ¯ k ) 2 N K ) × ( 1 n )

3. Results

As a rule, after feed provision, we observed decreased exploration, grooming, inactivity, crawling, swimming, and burrowing (P<0.05) (Figures 1A, 1B, 1C, 1D, 1E, and 1G, respectively) in all treatments. Exploration was more conspicuous prior to feeding (H = 1813.054; gl = 7; P≤0.05) with greater frequency rates when feed was provided at alternate days during the dark phase (3.95±2.86) and daily during the light phase (3.50±2.77) (Tukey's test at P<0.05) (Figure 1A). Grooming behavior mainly occurred prior to feeding (H = 633.533; gl = 7; P<0.05), especially in daily feed in light (4.72±3.73), daily feed in dark (4.87±4.30), and alternate feed in light (4.48±3.36) (P<0.05) (Figure 1B). Inactivity, crawling, and swimming had greater frequency rates prior to feeding for all treatments in the two phases (light/dark), with a decrease in frequency of such behaviors after feeding (P<0.05) (Figure 1C, 1D and 1E). Crawling occurred more frequently prior to feeding (H = 214.176; gl = 7; P≤0.001), with greater scores for alternate feeding in dark phase (AFD = 3.02±2.65) (Figure 1D). The above also occurred for swimming (H = 163.135; gl = 7; P≤0.001), mainly in treatments with feed restrictions (AFL and AFD) (Tukey's test at P<0.05) (Figure 1E). Results evidence behavior changes triggered by feed during the light and dark phases for the 24-h period.

Figure 1
Frequency (episodes.min−1) of behavior of Macrobrachium rosenbergii prawns (mean ± standard deviation) prior and after feeding in light and dark phases during a 24-h period.

Excavation of substrate mainly occurred prior to feeding, during the day light phase, with no statistical differences (H = 21.480; gl = 7; P = 0.003; post hoc Tukey's test, P<0.05), except for treatment with feeding on alternate days, during the day light phase (Figure 1F). Behavior burrowing in havens was observed in all treatments, with greatest frequency prior to feeding (H = 101.938; gl = 7; P≤0.001) and in the light phase (Tukey's test at P<0.05) (Figure 1G).

Agonistic behavior (Figure 1H) was reported in all treatments, regardless of photoperiod (light/dark), with significantly higher scores (H = 116.800; gl = 7; P≤0.001) for animals with feed restriction (AFL and AFD) (Tukey's test at P<0.05). Intake behavior prior to feeding was attributed to feed surplus on the substrate and seedlings in the experimental units. Higher intake rates were observed after feeding (H = 2414.529; gl = 7; P≤0.001), with higher means for treatment DFL, followed by AFL, DFD, and AFD (5.68±5.08, 3.38±4.77, 3.30±0.23, and 3.29±4.94, respectively) (Tukey's test at P<0.05) (Figure 1I).

Lesions and amputations in all body parts of farmed prawns were reported in all treatments. Pereiopods, pleopods, antennae, and uropods were the body limbs most affected by agonistic events. Highest rates of occurrences of lesions and amputations were reported for animals fed on alternate days, during the dark phase (Figure 2).

Figure 2
Number of lesions and amputations in body structures of M. rosenbergii prawns subjected to different feeding treatments.

The above result is corroborated by a great number of agonistic events by animals with feed restrictions (Figure 1H), coupled with the common occurrence of autotomy (self-amputation as an animal defense mechanism in conflict episodes). Although damages did not kill the animal, mutilated animals and animals with lesions depreciated the final product.

Full survival of animals was reported during the treatments under analysis, perhaps due to good water quality, feed amount, and the ability of prawns to acquire feed. There was a significant difference in the weight of animals every ten days of culture within the specific treatment. However, no difference between treatments was reported when they were compared on weighing days (T0, T10, T20, and T30) (Figure 3A). An apparent higher intake (g) was detected after feeding provision in all treatments when animals were subjected to feed restrictions (ANOVA, P≤0.001) (Figure 3B), resulting in lower feed efficiency (ANOVA, P = 0.859) (Figure 3C) and FCR (ANOVA, P = 0.222) (Figure 3D). Although no statistical difference was detected, a trend for greater feed efficiency and SGR was observed for daily treatments (DFL and DFD).

Figure 3
Weight (g), apparent intake (g) (mean ± standard deviation), feed efficiency, and feed conversion ratio of M. rosenbergii specimens subjected to different feeding treatments.

4. Discussion

Results showed that a short temporary restriction (24 h) in feed during light or dark phases did not affect survival, weight, feed efficiency, and SGR of M. rosenbergii. Feed intake had a higher rate in treatments to which animals were subjected with feed restriction during the light and dark phases when compared with those without any restrictions. Prawns reached similar weight and specific growth and survival rates. Since there was no difference between those subjected or not to temporary feed restriction, M. rosenbergii demonstrated good feed benefits within all the experimental conditions. Compensatory growth may be defined as past growth achieved after a period of fasting or reduced feed rates. In the case of aquatic animals, the strategy has been under observation over time (Weatherley and Gill, 1987Weatherley, A. H. and Gill, H. S. 1987. The biology of fish growth. Academic Press, London.; Broekhuizen et al., 1994Broekhuizen, N.; Gurney, W. S. C.; Jones, A. and Bryant, A. D. 1994. Modelling compensatory growth. Functional Ecology 8:770-782. https://doi.org/10.2307/2390237
https://doi.org/10.2307/2390237...
; Bull and Metcalfe, 1997Bull, C. D. and Metcalfe, N. B. 1997. Regulation of hyperphagia in response to varying energy deficits in overwintering juvenile Atlantic salmon. Journal of Fish Biology 50:498-510. https://doi.org/10.1111/j.1095-8649.1997.tb01945.x
https://doi.org/10.1111/j.1095-8649.1997...
; Rhaman et al., 2019Rahman, F.; Ghosh, A. K. and Islam, S. S. 2019. Effect of time-restricted feeding and refeeding regimes on compensatory growth, body composition, and feed utilization in prawn (Macrobrachium rosenbergii) culture system. Journal of Applied Aquaculture 1-14. https://doi.org/10.1080/10454438.2019.1661328
https://doi.org/10.1080/10454438.2019.16...
) due to its implication on fish farming and investigation on the biological phenomenon. However, the literature on prawns and on invertebrates subjected to feed restrictions is rather scarce.

According to Maclean and Metcalfe (2001)Maclean, A. and Metcalfe, N. B. 2001. Social status, access to food, and compensatory growth in juvenile Atlantic salmon. Journal of Fish Biology 58:1331-1346. https://doi.org/10.1006/jfbi.2000.1545
https://doi.org/10.1006/jfbi.2000.1545...
, animals subjected to feed restriction periods lose weight and growth is impaired. However, when feed is reestablished, the animals overeat and may achieve weight gain similar to those fed every day (control groups). In the case of shrimps, Maciel et al. (2018)Maciel, J. C.; Francisco, C. J. and Miranda-Filho, K. C. 2018. Compensatory growth and feed restriction in marine shrimp production, with emphasis on biofloc technology. Aquaculture International 26:203-212. https://doi.org/10.1007/s10499-017-0209-z
https://doi.org/10.1007/s10499-017-0209-...
reported that short fasting periods produced a greater efficiency in FCR for Litopenaeus vannamei, with decrease in phosphorus concentration in the water, due to excreta. Wu et al. (2001)Wu, L. X.; Dong, S. L.; Wang, F.; Tian, X. L. and Ma, S. 2001. The effect of previous feeding regimes on the compensatory growth response in Chinese shrimp, Fenneropenaeus chinensis. Journal of Crustacean Biology 21:559-565. https://doi.org/10.1163/20021975-99990157
https://doi.org/10.1163/20021975-9999015...
reported that groups of Fenneropenaeus chinensis subjected to fasting periods and re-feeding had compensatory growth, appetite, and overeating. The authors reported a compensatory growth in all groups subjected to restrictions and that, due to their previous nutritional record, prawns may regulate their appetite and growth rate. Pontes et al. (2010)Pontes, C. S.; Santos, D. B.; Bessa Júnior, A. P. and Arruda, A. M. V. 2010. Substituição de ração no crescimento de juvenis do camarão marinho Litopenaeus vannamei em laboratório. Revista Caatinga 23:121-126. analyzed temporary replacement of feed to shrimp by feed for broilers in the farming of L. vannamei to decrease costs, at short time intervals, and did not detect any difference in performance. In other words, parameters were not affected by the feed regime.

Few papers deal with feed restriction in fresh water prawns. Malecha et al. (1989)Malecha, S. R.; Sandifer, P. A.; Cotsapas, L.; Parseval, L.; D'Abramo, L.; MacMichael, E. R.; Desmond, T. and Zacarias, D. 1989. Potential application to Brazil of recent advances in the culture of marine shrimps and freshwater prawns. p.33-47. In: Anais do Brazilian Symposium on Prawn Culture. Associação Brasileira de Criadores de Camarão, João Pessoa. suggested the occurrence of compensatory growth in M. rosenbergii when small prawns, subjected to space restrictions, were separated from the original population or transferred to low stocking densities. Li et al. (2008)Li, Z.; Xie, S.; Wang, J. and Chen, D. 2008. Compensatory growth in shrimp Macrobrachium nipponense following starvation. Sichuan Journal of Zoology 27:335-339. tested feed restriction in Macrobrachium nipponense for 18 days in a laboratory and reported that animals with two- and four-day feed restriction had similar weight as those fed daily (control). Further, the authors observed that animals with feed restrictions decreased oxygen consumption and increased feed conversion efficiency as a compensatory effect.

Marques and Lombardi (2011)Marques, H. L. A. and Lombardi, J. V. 2011. Compensatory growth of Malaysian prawns reared at high densities during the nursery phase. Revista Brasileira de Zootecnia 40:701-707. https://doi.org/10.1590/S1516-35982011000400001
https://doi.org/10.1590/S1516-3598201100...
evaluated compensatory growth in post-larvae M. rosenbergii specimens cultivated at high densities (50, 400, 800, and 1200 prawns/m2) in net tanks during 244 days and reported that prawns farmed within the highest density showed a visible compensatory growth when compared with prawns in a density of 800 animals/m2. Ghosh et al. (2018)Ghosh, A. K.; Biswas, M.; Azad, M. A. K.; Islam, S. S.; Huq, K. A. and Shah, M. S. 2018. Effect of restricted feeding on growth performance and feed utilization of freshwater prawn (Macrobrachium rosenbergii) in pond aquaculture system. Khulna University Studies 15:13-22. reported that M. rosenbergii's growth rate increased significantly when the animals were subjected to a 50% feed restriction, albeit with significant effects on survival rate. More recently, Rahman et al. (2019)Rahman, F.; Ghosh, A. K. and Islam, S. S. 2019. Effect of time-restricted feeding and refeeding regimes on compensatory growth, body composition, and feed utilization in prawn (Macrobrachium rosenbergii) culture system. Journal of Applied Aquaculture 1-14. https://doi.org/10.1080/10454438.2019.1661328
https://doi.org/10.1080/10454438.2019.16...
found that feed restriction two days a week would not hamper the growth of M. rosenbergii, and followed by proper refeeding, feed could be restricted three days a week in improved traditional prawn culture. In addition, feed restriction does not hamper final production and showed a negligible reduction in protein content in body composition as well as better feed efficiency.

The current analysis demonstrated that prawns did not show any difference in final weight, feed efficiency, and SGR. Or rather, animals subjected to temporary feed restriction (fed on alternate days) had the same growth rate to those fed daily either in the light or in the dark phase of the 24-h period. El Ghazali et al. (2009)El Ghazali, I.; Saqrane, S.; Carvalho, A. P.; Ouahid, Y.; Oudra, B.; Del Campo, F. F. and Vasconcelos, V. 2009. Compensatory growth induced in zebrafish larvae after pre-exposure to a Microcystis aeruginosa natural bloom extract containing microcystins. International Journal of Molecular Sciences 10:133-146. https://doi.org/10.3390/ijms10010133
https://doi.org/10.3390/ijms10010133...
insisted that to obtain a compensatory growth, two phases are needed: a first stress phase during which animal growth is reduced, followed immediately by the second phase during which the growth depression disappears, allowing the resumption of growth, but at a rate below the animal's physiological capacity (compensatory growth). However, total or partial compensation depends on several factors, such as severity and duration of restriction, development stage of the organism, and re-feeding pattern (Wilson and Osbourn, 1960Wilson, P. N. and Osbourn, D. F. 1960. Compensatory growth after undernutrition in mammals and birds. Biological Reviews 35:324-361. https://doi.org/10.1111/j.1469-185X.1960.tb01327.x
https://doi.org/10.1111/j.1469-185X.1960...
; Ryan, 1990Ryan, W. J. 1990. Compensatory growth in cattle and sheep. Nutrition Abstracts and Reviews. Series B, Livestock Feeds and Feeding 60:653-664.).

Studies on the effects of fasting and re-feeding on the growth of prawns have revealed that hyperphagia is a mechanism that triggers compensatory growth (Wu et al., 2001Wu, L. X.; Dong, S. L.; Wang, F.; Tian, X. L. and Ma, S. 2001. The effect of previous feeding regimes on the compensatory growth response in Chinese shrimp, Fenneropenaeus chinensis. Journal of Crustacean Biology 21:559-565. https://doi.org/10.1163/20021975-99990157
https://doi.org/10.1163/20021975-9999015...
). Current experiment shows that prawns increased feed intake after diet provision. Intake is greater when animals fed daily during the light phase and may indicate that it is the preferential phase for diet provision. Since there is no difference in animal indexes among restriction and non-treatments, labor costs may be decreased through diet provision in alternate days. Barki et al. (1991)Barki, A.; Karplus, I. and Goren, M. 1991. Morphotype related dominance hierarchies in males of Macrobrachium rosenbergii (Crustacea, Palaemonidae). Behaviour 117:145-160. https://doi.org/10.1163/156853991X00508
https://doi.org/10.1163/156853991X00508...
observed that M. rosenbergii prawns compete for resources (feed, haven, and access to partners for mating) and that size and morphotype of males affect dominance hierarchy. More recently, Rahman et al. (2019)Rahman, F.; Ghosh, A. K. and Islam, S. S. 2019. Effect of time-restricted feeding and refeeding regimes on compensatory growth, body composition, and feed utilization in prawn (Macrobrachium rosenbergii) culture system. Journal of Applied Aquaculture 1-14. https://doi.org/10.1080/10454438.2019.1661328
https://doi.org/10.1080/10454438.2019.16...
found that when feed is provided, mainly to groups subjected to temporary feed restriction, competition among the animals ensued.

Agonistic behavior mainly occurs in treatments when feed is given at alternate days, prior to and after feed provision, during the light and dark phases. The above indicates that feed restriction escalates the aggressiveness of M. rosenbergii and may interfere in the quality of the final product. These data are corroborated by Short (2004)Short, J. W. 2004. A revision of Australian river prawns, Macrobrachium (Crustacea: Decapoda: Paleomonidade). Hydrobiologia 525:1-100. https://doi.org/10.1023/B:HYDR.0000038871.50730.95
https://doi.org/10.1023/B:HYDR.000003887...
and Balasundaram et al. (2004)Balasundaram, C.; Jeyachitra, P. and Balamurugan, P. 2004. Shelter preference in Macrobrachium spp. with reference to aquaculture. Acta Ethologica 7:95-101. https://doi.org/10.1007/s10211-004-0090-4
https://doi.org/10.1007/s10211-004-0090-...
who stated that Macrobrachium prawns are nocturnal, aggressive, and territorial, preferring havens during the day. As a rule, animals compete to achieve resources (havens, feed, and mates), whilst one of the most obvious mechanisms to this end is aggressiveness (Martin and Moore, 2007Martin, A. L. and Moore, P. A. 2007. Field observations of agonism in the crayfish, Orconectes rusticus: shelter use in a natural environment. Ethology 113:1192-1201. https://doi.org/10.1111/j.1439-0310.2007.01429.x
https://doi.org/10.1111/j.1439-0310.2007...
).

Specimens in all treatments seek havens during the light day period. Havens are relevant resources to increase access to mates and to minimize aggressive encounters and predation. They provide protection to subdued animals in the presence of dominant animals (Englund and Krupa, 2000Englund, G. and Krupa, J. J. 2000. Habitat use by crayfish in stream pools: influence of predators, depth and body size. Freshwater Biology 43:75-83. https://doi.org/10.1046/j.1365-2427.2000.00524.x
https://doi.org/10.1046/j.1365-2427.2000...
; Martin and Moore, 2007Martin, A. L. and Moore, P. A. 2007. Field observations of agonism in the crayfish, Orconectes rusticus: shelter use in a natural environment. Ethology 113:1192-1201. https://doi.org/10.1111/j.1439-0310.2007.01429.x
https://doi.org/10.1111/j.1439-0310.2007...
; Alcock, 2011Alcock, J. 2011. Comportamento animal. Uma abordagem evolutiva. 9.ed. Artmed, Porto Alegre.). Current authors reported that, prior to feed provision, the animals showed higher behavior rates, such as grooming, excavation, and crawling. According to Bauer (1989)Bauer, R. T. 1989. Decapod crustacean grooming: functional morphology, adaptive value, and phylogenetic significance. p.49-73. In: Functional morphology of feeding and grooming in Crustacea. Felgenhauer, B. E.; Watling, L. and Thistle, A. B., eds. Crustacean Issues 6. A. A. Balkema, Rotterdam., several decapod crustacean species spend much time and energy in grooming. High exploration and crawling rates prior to feed provision are natural seeking for food. These types of behavior have been detected for the prawn species L. vannamei (Pontes et al., 2006Pontes, C. S.; Arruda, M. F.; Menezes, A. A. L. and Lima, P. P. 2006. Daily activity pattern of the marine shrimp Litopenaeus vannamei (Boone 1931) juveniles under laboratory conditions. Aquaculture Research 37:1001-1006. https://doi.org/10.1111/j.1365-2109.2006.01519.x
https://doi.org/10.1111/j.1365-2109.2006...
). Feeding occurred in the light and dark phases and corroborated current results. Nunes et al. (1996)Nunes, A. J. P.; Goddard, S. and Gesteira, T. G. V. 1996. Feeding activity patterns of the Southern brown shrimp Penaeus subtilis under semi-intensive culture in NE Brazil. Aquaculture 44:371-386. https://doi.org/10.1016/0044-8486(96)01297-5
https://doi.org/10.1016/0044-8486(96)012...
and Pontes and Arruda (2005)Pontes, C. S. and Arruda, M. F. 2005. Comportamento de Litopenaeus vannamei (Boone) (Crustacea, Decapoda, Penaeidae) em função da oferta do alimento artificial nas fases claras e escuras do período de 24 horas. Revista Brasileira de Zoologia 22:648-652. https://doi.org/10.1590/S0101-81752005000300019
https://doi.org/10.1590/S0101-8175200500...
reported that prawns of the species Farfantepenaeus subtilis and L. vannamei, respectively, fed during the day and during the night.

Feed restriction in species with territorial behavior may trigger serious conflicts, with loss of limbs and even death. The current research showed that, although no death occurred in any of the treatments, lesions and amputations were common, especially in animals subjected to temporary feed restriction. Karplus et al. (1989)Karplus, I.; Samsonov, E.; Hulata, G. and Milstein, A. 1989. Social control of growth in Macrobrachium rosenbergii. I. The effect of claw ablation on survival and growth of communally raised prawns. Aquaculture 80:325-335. https://doi.org/10.1016/0044-8486(89)90179-8
https://doi.org/10.1016/0044-8486(89)901...
reported that the lack of chelae (second pair of pereiopods) suppressed aggressiveness in adult M. rosenbergii and M. amazonicum, respectively. The authors detected that agonistic behavior in almost all reports was performed by the second pair of pereiopods. Karplus et al. (1992)Karplus, I.; Hulata, G.; Ovadia, D. and Jaffe, R. 1992. Social control of growth in Macrobrachium rosenbergii. III. The role of claws in bull-runt interactions. Aquaculture 105:281-296. https://doi.org/10.1016/0044-8486(92)90093-Z
https://doi.org/10.1016/0044-8486(92)900...
reported a significant increase in the survival of male M. rosenbergii featuring orange-colored and transparent chelae when dominant males (blue chelae) did not have any chelae. Brugiolo et al. (2007)Brugiolo, S. S. S.; Barbosa, J. M.; Hernandez Blazquez, F. J. and Nascimento, P. A. M. 2007. Canibalismo em fêmeas de Macrobrachium rosenbergii (De Man, 1879) (Crustacea, Palaemonidae): efeito da retirada das quelas. Revista Portuguesa de Ciências Veterinárias 102:153-157. suggested that the removal of chelae in M. rosenbergii is viable in commercial prawn farms, even though it entails more technical labor.

The data above show that repeated cycles of short fasting and feeding may be a useful protocol to improve the use of feed and to decrease labor costs in feed management. Field studies with M. rosenbergii populations in monosex farming may elucidate other aspects on the physiology, behavior, and growth of the animals.

5. Conclusions

Short feed restriction with feed provision on alternate days may be employed without any impairment to growth and survival of the animals. Apparent intake of feed increases after provision on alternate days, coupled to low feed conversion ratio and specific growth rate during the light and dark phases. It should be highlighted that increase in aggressive behavior and, consequently, in the number of lesions and amputations indicates low welfare conditions of M. rosenbergii and depreciation in the quality of the final product.

Acknowledgments

The present work was supported by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Brasil (CAPES) – financing code 001.

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Publication Dates

  • Publication in this collection
    16 Sept 2020
  • Date of issue
    2020

History

  • Received
    08 July 2019
  • Accepted
    09 June 2020
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