ANIMAL WELFARE ASPECTS OF HUSBANDRY SYSTEMS FOR FARMED FISH: CARP 1. Scientific Opinion of the Panel on Animal Health and Welfare

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1 The EFSA Journal (2008) 843, 1-28 ANIMAL WELFARE ASPECTS OF HUSBANDRY SYSTEMS FOR FARMED FISH: CARP 1 Scientific Opinion of the Panel on Animal Health and Welfare (Question N EFSA-Q ) Adopted on the 22 nd of October For citation purposes: Scientific Opinion of the Panel on Animal Health and Welfare on a request from the European Commission on animal welfare aspects of husbandry systems for farmed fish: carp. The EFSA Journal (2008) 843, 1-28 European Food Safety Authority, 2007

2 PANEL MEMBERS Bo Algers, Harry J. Blokhuis, Donald M. Broom, Patrizia Costa, Mariano Domingo, Mathias Greiner, Daniel Guemene, Jörg Hartung, Frank Koenen, Christine Müller-Graf, David B. Morton, Albert Osterhaus, Dirk U. Pfeiffer, Ron Roberts, Moez Sanaa, Mo Salman, J. Michael Sharp, Philippe Vannier, Martin Wierup. A minority opinion was expressed by Prof. Donald Broom, member of the AHAW panel, based on the view that the accepted Report and adopted Opinion are incomplete. According to Prof. Broom introductory chapters on welfare, biological functioning and farming of fish should be included to the report in order to answer the mandate from the European Commission. The EFSA Journal (2008) 843, 2-28

3 SUMMARY Following a request from European Commission, the Panel on Animal Health and Welfare was asked to deliver a scientific opinion on animal welfare aspects of husbandry systems for farmed fish. Council Directive 98/58/EC concerning the protection of animals kept for farming purposes lays down minimum standards for the protection of animals, including fish. The Scientific Opinion on welfare of carp was adopted on 22 October The common carp (Cyprinus carpio, Linnaeus 1758), which is by far the species farmed in largest numbers, is the scope of this opinion. Common carp is a domesticated species that has well adapted to the husbandry systems within which it is reared. In Europe, only two major production systems (monoculture of carp and polyculture of carp) are commonly practised. There are numerous combinations of polyculture with common carp production. Since the species involved are all cyprinids and occupy only slightly different ecological niches in the pond system, they were subjected to the same risk and hazard assessments as carp in monoculture. Consequently, for the purpose of risk assessment, polyculture was considered as an intensive monoculture production system. The various life stages of carp considered are: fertilised eggs and embryos, yolk sac fry, free swimming fry, nursed fry, fingerling, overwintering carp, on-growers, marketable fish, and broodstock. A review of environmental conditions and factors that were identified as possibly affecting the welfare of common carp, Cyprinus carpio, at different life stages has been conducted. These factors are grouped as: abiotic and biotic factors (including behavioural interactions), food and feeding, husbandry and management, genetics, and the impact of disease and disease control measures. It is however important to realise that the environmental conditions are always defined by a range of inter-related factors. While each specific variable is described separately, there are very few occasions in reality where only a single factor is involved in any fish welfare issue relating to environmental conditions. For this reason, only ranges of acceptable levels for the various factors can be given and these should always be considered in the context of the other variables involved. A semi-quantitative risk assessment was carried out to obtain a ranking of risk for different life stages under different production systems. Light levels applied to embryos should be kept low to avoid over-stimulation leading to exhaustion of endogenous reserves. The anatomy of carp may render them particularly vulnerable to excessive noise and vibration. There are no water flow requirements under carp farming conditions (except for eggs). Cessation of water flow helps hatching. Excessive water flows may cause crowding of fry and wasted use of energy reserves leading to starvation. Too low water flow was found in the risk assessment to be a more highly ranked hazard (causing hypoxia) in early life stages. Carp are remarkably tolerant to low oxygen levels, except in the first few months of the life cycle when fry are more sensitive. Occasionaly severe oxygen depletion associated with collapse of algal blooms in late summer at high temperatures can affect welfare. However, the results of the risk assessment found low oxygen to be the most The EFSA Journal (2008) 843, 3-28

4 important or second most important hazard for all life stages. Fry is a life stage particularly sensitive to low but also high O 2 levels. The risk assessment scoring found low oxygen to be an important cause of mortality at all life stages; but low oxygen levels are most important in the early stages. Eggs exposed to levels of gas supersaturation can lead to long term effects on surviving individuals. Supersaturation of dissolved gases may lead to gas bubble formation inside the larvae causing disruption of swimming activity. Carp can survive across a wide temperature range by adjustment of their level of activity. Carp larvae are very susceptible to temperature fluctuations: excessively high temperatures lead to increased rates of body deformities. Rapid temperature changes rather than absolute limits are normally a significant welfare issue for carp fry. Rapid temperature change was found in the risk assessment to be an important hazard for yolk and nursed fry and fingerlings. During incubation high water ph can lead to incomplete embryonic development and deformities and was found in the risk assessment to be an important hazard. Carp larvae are particularly sensitive to acid stress. In later life stages, water ph per se has little importance in carp husbandry, it is only important in terms of its influence on other abiotic hazards (e.g. ammonia) should they be present. Carp are not affected by suspended solid levels except at the very high concentrations that may occur during harvesting. High suspended solids can suffocate eggs and embryos (it was the third highest ranked hazard for this life stage) and the water supply to the hatchery water should be filtered to limit suspended solid and predatory invertebrates. Unionised ammonia can be a serious welfare issue under conditions of intensive photosynthesis such as following collapse of algal blooms. This was reflected in the risk assessment tables where unionised ammonia was highly ranked in nearly all life stages. A great care and understanding is required in levels of fertiliser in ponds to avoid this hazard. In the present culture systems in Europe, overwintering ponds do not present a particular welfare risk, compared with other life stages, although it is important that these overwintering ponds are sufficiently deep for the coldest weather. Catch pits in harvest ponds should be carefully designed to minimise the suspended solids problems. For larvae, bad design of the tank would prevent the swim bladder filling with air resulting in incomplete development of the swim bladder, impaired swimming ability, poor health and slow growth rates. Unless ponds are managed carefully, anoxic layers producing toxic metabolites can develop. Algal blooms can be a significant welfare risk because of their effect on ph, because the algae may themselves be toxic, and because the collapse of algal blooms may cause severe and acute anoxia. The results of the risk assessment indicated that algal blooms were most important during the on-growing stage. Predation is a very serious welfare issue particularly significant in the farm pond environment where cormorants in particular can induce significant stress to the fish manifested by behavioural modifications and associated reduction in feeding, and the birds may also inflict injury. The EFSA Journal (2008) 843, 4-28

5 Whilst carp generally feed on natural feed, above certain densities they should receive supplementation with a correctly balanced feed for a fish that already feed on natural feed. Stocking fry into ponds with insufficient supplies of suitable food will result in low survival rates, poor growth and significant deformities. Food supply is the main factor governing appropriate stocking density. This was reflected in the risk assessment results: a shortage of natural food was the highest ranked hazard for the free and nursed fry stage. Disease is one of the major welfare issues in all fish husbandry. In the case of carp it is particularly related to environment. Most carp pathogens are facultative pathogens present in the environment. Those diseases with chronic, often sub-clinical effects are often of greatest welfare significance. In more acute conditions, control or treatment measures may have significant welfare impact in their own right. Good husbandry should be the major means of disease control. Currently very few of the treatments which are effective can be used due to the fact that they are not licensed. The risk assessment scored three selected diseases. These hazards affected mainly the earlier life stages (fry) and their importance varied between production systems. Key words: carp, animal welfare, risk assessment, fish farming, husbandry system, aquaculture, environmental conditions, biotic factors, feeding, husbandry, disease. The EFSA Journal (2008) 843, 5-28

6 TABLE OF CONTENTS Panel Members...2 Summary...3 Table of Contents...6 List of tables...8 Background as provided by european commission...9 Terms of reference as provided by european commission...9 Acknowledgements...9 Outcomes from the data presented in the scientific report Common carp, its importance to European aquaculture Overview of carp production systems in Europe Factors affecting the welfare of carp Abiotic factors Light period and intensity Noise and vibration Water flow Water oxygen content Total dissolved gases Water temperature Water ph Suspended solids Ammonia content Pond size and morphology Substrate of ponds Environmental pollutants Environmental conditions biotic factors Algal blooms Behavioural interactions Predation Stocking density Food and feeding Husbandry and management Handling of broodstock On-farm movements Sorting and Grading Monitoring Staff training on welfare Genetics Impact of diseases on welfare Diseases control measures Biosecurity Monitoring mortalities / survival rates Drug usage Vaccination Risk assessment approach to welfare of common carp Eggs Yolk sac fry Free living fry Nursed fry Fingerlings Over-wintering On-growers...19 The EFSA Journal (2008) 843, 6-28

7 4.8. Marketable fish Broodstock Uncertainty Mortality General discussion Risk mitigation / Recommendations...23 Conclusions and recommendations...24 The EFSA Journal (2008) 843, 7-28

8 LIST OF TABLES Table 1: Welfare risk ranking: eggs Table 2: Welfare risk ranking: yolk sac fry Table 3: Welfare risk ranking: free living fry Table 4: Welfare risk ranking: nursed fry/nursing Table 5: Welfare risk ranking: fingerling Table 6: Welfare risk ranking: over wintering Table 7: Welfare risk ranking: on growing Table 8: Welfare risk ranking: marketable fish Table 9: Welfare risk ranking: broodstock Table 10: Mortality scores >4 and 5 for the top 6 ranked hazards for each life stage The EFSA Journal (2008) 843, 8-28

9 BACKGROUND AS PROVIDED BY EUROPEAN COMMISSION Council Directive 98/58/EC concerning the protection of animals kept for farming purposes lays down minimum standards for the protection of animals bred or kept for farming purposes, including fish. In recent years growing scientific evidence has accumulated on the sentience of fish and the Council of Europe has in 2005 issued a recommendation on the welfare of farmed fish 2. Upon requests from the Commission, EFSA has already issued scientific opinions which consider the transport 3 and stunning-killing 4 of farmed fish. TERMS OF REFERENCE AS PROVIDED BY EUROPEAN COMMISSION In view of this and in order to receive an overview of the latest scientific developments in this area the Commission requests EFSA to issue a scientific opinion on the animal welfare aspects of husbandry systems for farmed fish. When relevant, animal health and food safety aspects should also be taken into account 5. This scientific opinion should consider the main fish species farmed in the EU, including Atlantic salmon, gilthead sea bream, sea bass, rainbow trout, carp and European eel and aspects of husbandry systems such as water quality, stocking density, feeding, environmental structure and social behaviour. Due to the great diversity of species it was proposed that separate scientific opinions on species or sets of similar species would be more adequate and effective. It was agreed to subdivide the initial mandate into 5 different questions in relation to Atlantic salmon, trout species, carp, sea bass and gilthead sea bream, and in relation to European eel This Scientific Opinion refers only to carp. ACKNOWLEDGEMENTS The European Food Safety Authority wishes to thank the members of the Working Group for the preparation of this opinion: Ronald Roberts (Chairman), Edmund Peeler (Risk Assessor), Zdenek Adamek, Alan Henshaw, Zsigmond Jeney, Maciej Pilarczyk, Rodney Wootten, and Felicity Huntingford. The scientific report was reviewed by Flavio Corsin. 2 Recommendation concerning farmed fish adopted by the Standing Committee of the European Convention for the protection of animals kept for farming purposes on 5 December Opinion adopted by the AHAW Panel related to the welfare of animals during transport -30 March Opinion of the AHAW Panel related to welfare aspects of the main systems of stunning and killing the main commercial species of animals- 15 June Food Safety aspects of fish welfare are addressed by a Scientific Opinion of the BIOHAZ Panel ( Food Safety aspects of Animal welfare aspects of husbandry systems for farmed fish, Question N EFSA-Q ). The EFSA Journal (2008) 843, 9-28

10 OUTCOMES FROM THE DATA PRESENTED IN THE SCIENTIFIC REPORT 1. Common carp, its importance to European aquaculture The family Cyprinidae is the most important in numbers of species of all freshwater teleosts. The Common Carp (Cyprinus carpio, Linnaeus 1758) is one of the most widespread members of the Cyprinid family. In Europe, the common carp is by far the carp species farmed in largest numbers. However, due to socio-economical changes in Central and Eastern Europe, the production of common carp has declined sharply, between 1990 and Carp production in Europe is currently of about metric tons and 90% of this is produced by aquaculture. 2. Overview of carp production systems in Europe Carp are omnivorous fish with a strong tendency to eat animal food. Carp occur naturally in summer-warm lakes and slowly flowing rivers. Carp are rarely found in clear, cool, swift-flowing streams. They prefer muddy areas where they search for food organisms. Carp can tolerate winter temperatures below 2 C. They can tolerate temperatures above 30 C for short periods. The scientific report, which was used as a basis for this opinion defines the systems used for culture of the common carp, and highlights areas where such systems may increase the likelihood of negative effects on the welfare of carp. Three main production systems of common carp can be differentiated as: i) monoculture of carp, ii) polyculture of carp, and iii) integrated carp culture with other agricultural activities. There are very few intensive systems in the region despite existing technology. As a simplification, carp polyculture will be considered as an intensive monoculture production system, only considering the number of individuals not their species richness. There is very little scientific literature that specifically addresses the welfare of carp under farming conditions. 3. Factors affecting the welfare of carp The various life stages of carp considered are: fertilised eggs and embryos, yolk sac fry, free swimming fry, nursed fry, fingerling, overwintering carp, on-growers, marketable fish, and broodstock. A review of environmental conditions and factors that were identified as possibly affecting the welfare of common carp at different life stages has been conducted. These factors are grouped as: abiotic and biotic factors (including behavioural interactions), food and feeding, husbandry and management, genetics, and the impact of disease and disease control measures. It is however important to realise that the environmental conditions are always defined by a range of inter-related factors. While each specific variable is described separately, there are very few occasions in reality where only a single factor is involved in any fish welfare issue relating to environmental conditions. For this reason, only ranges of acceptable levels for the various factors can be given and these should always be considered in the context of the other variables involved. The EFSA Journal (2008) 843, 10-28

11 3.1. Abiotic factors Light period and intensity Carp, like all cyprinid fish, react to changes in light. Change in photoperiod regime may affect carp growth rate, maturation and spawning alacrity, and respiration. During the main part of the production cycle, when the carp are held in extensive earth ponds, fish are exposed to a natural photoperiod, which is associated with other environmental features, such as temperature. For eggs and larvae, expert opinion suggests that light levels should be kept low to avoid stimulation of the embryo Noise and vibration There is evidence that cyprinids are sensitive to noise and vibration. Carp physoclistous swim bladder makes this fish susceptible to major vibrations Water flow Common carp do not require flowing water. In farming conditions carp are produced in ponds without water flow, except for replacement of water losses due to seepage or evaporation. For young stages, water flows in excess of these rates may cause shock and trauma, as well as exhaustion Water oxygen content Carp are remarkably tolerant to low oxygen levels, except in the first few months of the life cycle when fry are more sensitive Total dissolved gases Expert opinion indicates that above a 100% level of total dissolved gases, problems can occur with gas bubble formation leading to a loss of eggs and larvae Water temperature Carp are able to survive across a wide temperature range (from ~2 C to > 36 C), although activity changes drastically with temperature. Decreases in water temperature below 20 C and increases above 30 C both lead to a decline in feeding. During the incubation of eggs, it is important that the temperature of the water be maintained as constant as possible within the optimal range. Carp larvae are very susceptible to temperature fluctuations Water ph Adult carp can survive in waters with a wide range of ph , although extreme values reduce feeding activity and thus growth rates. The direct effect of ph is less important than the indirect effect of increased ph values have on the un-ionized ammonia content. The EFSA Journal (2008) 843, 11-28

12 Suspended solids Feeding activity of carp causes re-suspension of bottom sediments, resulting in high concentrations of suspended solids. In case of excessive suspended solids severe gill obstruction occurs and there is considerable reduction in respiratory capacity, limited gas exchange across the gills and temporary anoxia. Water supplies to the egg incubation system, should be filtered to remove any particulate organic or inorganic material. This also ensures no predatory invertebrates such as cyclopoid copepods are present in the hatchery tanks Ammonia content The toxicity caused by ammonia is related to the level of unionized ammonia (NH 3 ) and this varies depending on the ph of the water and also temperature, with lower temperatures resulting in lower levels of unionised ammonia. Under normal carp culture conditions, total ammonia nitrogen levels rarely exceed 1-2 mg/l so welfare issues rarely arise except in case of intensive photosynthesis by blooming algae Pond size and morphology Since carp are grown in large to very large ponds or even small lakes, their conditions in many ways mirror those of their natural environment. Depending on pond size, depth and stocking density, ponds can vary in their complexity. Provision of a drainage chamber and catch pit and a controlled method of removing the water will reduce the stress associated with harvesting. Design of tanks is important to the swim up of larvae Substrate of ponds The feeding activity of carp tends to remove all vegetation from the pond bottom and the constant stirring leads to the formation and deposition of a fine sediment. Silt can build up to a considerable depth and lower layers of this silt, if undisturbed, become anoxic. This favours the production of toxic substances. For over-wintering carp, the substrate should not have a high organic content as this may increase oxygen consumption within the substrate and production of toxic gases Environmental pollutants Carp ponds are relatively stable and do not normally have any substantial water inflow, but there is some replacement water for evaporation and rain can bring terrestrial pollutants into the system Environmental conditions biotic factors Algal blooms Algal blooms may affect welfare of fish in three different ways. First, because their photosynthesis levels are so high, their metabolites can cause dramatic increases in pond ph to levels that may be toxic either directly or through increases the proportion of unionized ammonia to toxic levels. Secondly, in many cases the algae involved may The EFSA Journal (2008) 843, 12-28

13 include toxigenic cyanobacterial species, which can on occasion cause mass mortality. Thirdly, when the bloom collapses, the oxygen may be extracted from the water column at a very rapid rate, and this can lead to significant mortality Behavioural interactions In general, the senses of common carp are the same as for other fish. Common carp usually establish well-defined home ranges. During winter, over-wintering ponds may not offer the fish scope for movement and continued feeding. In polyculture interactions with other species include potential competition for food and, more importantly in a welfare context, predation Predation Especially when small, carp fall prey to a wide variety of predators including mammals, birds, other fish and also invertebrates. Predation is a serious welfare issue and stress is manifested by behavioural modifications and associated reduction in feeding Stocking density Stocking levels in carp pond vary depending on the farming system, the nature of the pond, whether it is winter or summer and whether there is to be auxiliary feeding Food and feeding Because carp are almost exclusively produced in semi-intensive pond farms or under extensive conditions, feeding is only practised to complement the energy and protein requirements provided by pond primary production Husbandry and management Stocking in outdoor ponds is a stressful experience for fish at all stages of development, but the early life stages are particularly sensitive and susceptible to environmental change. Newly-hatched larvae are extremely fragile and should never be removed from water. Transport to the pond should be done as quickly as possible and with the minimum of handling. Great care should be taken to ensure that the fish are not subjected to a rapid change in water parameters. Acclimation can be achieved by introducing the fish gradually to the environmental conditions present in the receiving tank or pond. Harvesting is another critical phase of carp culture Handling of broodstock Spawners need to be separated by sex when water temperatures rise. After separation, feeding is increased. Spawners are moved into the hatchery. Fish are examined and the ripe developed specimens selected. Induced ovulation of spawners is done in tanks or in special small ponds. Fish are generally anaesthetized. Hypophysation is the traditional method of inducing fish to spawn and is widely practised in carp culture. The sexual products stripped from the fish are mixed and a fertilizing solution is added to prevent egg agglomerating. Spawners should be kept undisturbed between the treatments and ovulation. The EFSA Journal (2008) 843, 13-28

14 On-farm movements On-farm movements are movements of fish within the aquaculture facility tend to short term in nature usually lasting less than 30 min. Because of the temporary nature of the activity, welfare issues are generally limited to physical damage, dissolved oxygen content of the transport water, nature and levels of suspended solids and temperature shocks experienced when transferring the fish from one water body to another. Open tanks with aeration can be used. At temperatures above 15 C low doses of anaesthetic can be used to tranquilise the carp. During on farm transport operations, it is common practice to add low concentrations of NaCl to the transport water in order to minimise stress Sorting and Grading Sorting and grading happen at different times in the production cycle. Polyculture is widely practised in European carp culture and, after being removed from the pond, the fish are placed onto sorting tables where the individual species and size groups can be separated. Most of this separating and sorting is done by hand although increasingly, the fish are graded using mechanical graders, which tend to cause less damage Monitoring Frequent monitoring of the water quality is essential as there are a number of variables that affect the well-being of fish. In culture systems, the main factors that need to be monitored are temperature, dissolved oxygen, ph and the metabolic by-products NH 3 and NO 2. Depending on the culture system used, other parameters that need monitoring may include alkalinity, PO 4, total phosphorus, NO 3, CO 2, Biochemical and Chemical Oxygen Demand (BOD, COD), and turbidity. In addition to water quality, information is also needed on feed rates, growth, condition, mortalities, disease status and ultimately survival rates. These data enable the farmer to make informed husbandry decisions and ensure the continued health and welfare of the fish Staff training on welfare To be successful and to maintain welfare standards in carp culture, it is important that staff at each unit is experienced and proficient. Failure to invest in the training and development of staff can lead to fish being subjected to avoidable stressors such as overcrowding, poor handling, underfeeding, sub-optimal culture conditions and inappropriate disease treatment Genetics Quality breeding programs exist for common carp. Many varieties and strains of scaly or mirror carp (with some large shining scales), including hybrids, are available. Common carp is a domesticated species that well adapted to the husbandry systems within which it is reared Impact of diseases on welfare Disease is one of the major welfare issues in all fish husbandry. In the case of carp it is particularly related to environment. Most carp pathogens are facultative pathogens present The EFSA Journal (2008) 843, 14-28

15 in the environment. Those diseases with chronic, often sub clinical effects are often of greatest welfare significance. In the case of more acute conditions, control or treatment measures may have significant welfare impact in their own right. Good husbandry should be the major means of disease control Diseases control measures Biosecurity Biosecurity covers implementation of a set of programmes and procedures preventing the entry, establishment or spread of unwanted pests and infectious disease agents whether they are a risk to humans, animals, plants or the environment. Biosecurity is the state of having applied appropriate measures to prevent or limit the possibility of pathogens entering populations from an exogenous source Monitoring mortalities / survival rates Mortalities of fish during the production cycle can result from a variety of causes, including, disease, predation, damage, and adverse environmental conditions. Very poor welfare (e.g. disease, poor growth and mortalities) is not cost-effective for the farmer. At present many farms rely on the experience of the farm manager to decide when mortalities require additional action Drug usage Carp diseases are a significant welfare hazard but currently very few of the treatments which are effective are used due to the fact that these veterinary medicinal products are not authorised Vaccination As with any animal husbandry system, the intensification of fish farming has inevitably resulted in the emergence of disease problems, infectious diseases in particular. Carp farming is still to a large extent extensive, but in the case of Koi carp, for example, the value of the commercial product is now recognised as being worth treating with more expensive antibiotics or vaccines. Vaccines have made a significant contribution to controlling serious infectious diseases of fish. Future research on effective vaccination of carp against major infectious diseases is recommended as a means of improving carp welfare in this regard. 4. Risk assessment approach to welfare of common carp The risk scores based on expert advice were used to compile a risk ranking by category such as abiotic or biotic to obtain an idea which hazards are the more important for each life stage in the various production systems considered, and also to enable the comparison of the different production systems. The EFSA Journal (2008) 843, 15-28

16 4.1. Eggs The important hazards for both Dubish ponds and jars were water quality parameters. The highest ranked hazards were low water oxygen content for jars and low water temperature in Dubish ponds. Too high or too low water flows were important in jars whilst only low water flow was important in Dubish ponds. High suspended solids ranked higher in jars (3) compared with Dubish ponds (8). The highest ranked hazards all lead to deformities which would persist through to later life stages. The top three ranked hazards also caused significant levels of mortality (greater than 40%). Water quality parameters score highly in part, because a high proportion of the population is affected (all the top hazards affected >40% of the populations and most affected greater than 60%). The most frequently occurring hazard was low water oxygen in Dubish ponds (low probability); all other highly ranked hazards occurred with very low or extremely low frequency. Table 1: Welfare risk ranking: eggs Jars Dubish Pounds water oxygen content too low water flow too low suspended solids too high water temperature too low / unionised ammonia content water temperature too low water oxygen content too low water flow too low water oxygen content too high / water temperature rapid change / water ph too high water flow too high 4.2. Yolk sac fry Water quality parameters remained important for yolk sac fry in both tanks/troughs and Dubish ponds, notably low water oxygen and low water temperature. There were some interesting differences between the 2 systems. White spot disease was the highest ranked risk in Dubish ponds and only the 8 th ranked risk in tanks. Poor handling was important in jars but not Dubish ponds. The highest ranked hazards all resulted in deformities, have high severity scores and affect a high proportion of the population However, the probability of occurrence of hazards occurring was extremely or very low. The EFSA Journal (2008) 843, 16-28

17 Table 2: Welfare risk ranking: yolk sac fry Trough or Tank water oxygen content too low water flow too low suspended solids too high water oxygen content too high / handling not in acorrdance with best practice White Spot Disease Dubish ponds water oxygen content too low / water temperature too low unionised ammonia content water oxygen content too high / water temperature rapid change water temperature too low / unionised ammonia content 4.3. Free living fry The top ranked hazards in all three systems were similar. Whilst water parameters remain important, shortage of natural food is the most important hazard for all systems. This hazard results in deformities. The hazard attains a high score because its severity is high, and it affects a high proportion of the population. The dependence of the life stage on natural food means that intervention to mitigate the impact is limited. Water quality parameters and temperature (too high or too low), white spot and Saprolegnia are important in all three systems. Inappropriate design of the pond was considered an important hazard for all three systems. Too high a temperature was the hazard with the highest probability of occurrence which had a low probability. Table 3: Welfare risk ranking: free living fry Dubish ponds Nursing ponds Fingerling ponds shortage of natural food long term water temperature too high / water oxygen content too low / water temperature too low shortage of natural food long term water temperature too high / water oxygen content too low / water temperature too low shortage of natural food long term water temperature too high / water oxygen content too low / water temperature too low pond size, morphology and substrate / water ph too low / water ph too high / White Spot Disease pond size, morphology and substrate / White Spot Disease / Saprolegnia pond size, morphology and substrate /White Spot Disease / Saprolegnia The EFSA Journal (2008) 843, 17-28

18 4.4. Nursed fry For both production systems, a lack of food supply continues as the most important hazard from the free living to the nursed fry stage. The hazards are very similar for both systems: low water oxygen, too low temperature and high unionised ammonia content. The main impact of the top ranked hazards remains deformities. The highest ranked hazards had high severity scores and affected a high proportion of the population, but occurred with very low or extremely low probability. Table 4: Welfare risk ranking: nursed fry/nursing Nursing Pond shortage of natural food long term water oxygen content too low /water temperature too low unionised amonia content Fingerling Pond shortage of natural food long term water oxygen content too low / water temperature too low unionised amonia content water temperature too high water flow too low / water temperature rapid change / water ph too low / water ph too high / suspended solids too high water temperature too high water flow too low / water temperature rapid change / water ph too low / water ph too high / suspended solids too high 4.5. Fingerlings At this life stage there is only one production system. The top three hazards remain the same as the previous life stage. A long term shortage of food is the 4 th highest ranked hazards. At this life stage hazards result in reduced growth and poor condition (as well as mortality). The hazard which occurred with the highest probability was low oxygen (low probability). Predation also occurred with low frequency, and resulted in considerable mortality. Its severity at this life stage is low since mortality was the most common outcome, not injury. On some farms predation will occur with moderate or high frequency. Table 5: Welfare risk ranking: fingerling water oxygen content too low Fingerling Ponds water temperature too low unionised amonia content to high shortage of natural food long term The EFSA Journal (2008) 843, 18-28

19 water temperature too high / water temperature rapid change 4.6. Over-wintering Over-wintering carp may be kept in over-wintering or grow-out ponds but the most important hazards are the same: low water oxygen, predators and low water flow (leading to hypoxia). Hypoxia results in stress and mortalities. Predation can lead to mortalities but from a welfare point of view, stress and physical damage to survivors can also occur. Too low temperature or rapid changes in temperature were highly ranked because they may lead to stress. There are clearly interactions between some hazards. Stress may result in an increased risk of disease as well as directly affecting the carp s welfare. Table 6: Welfare risk ranking: over wintering Over wintering ponds water oxygen content too low predators water flow too low water temperature rapid change / water temperature too low / unionised ammonia content Grow out ponds water oxygen content too low water flow too low predators water temperature rapid change / water temperature too low / unionised ammonia content 4.7. On-growers On-growers may be kept under intensive or extensive conditions. Interestingly, a very similar ranking of hazards are found in both systems: low water oxygen, rapid change in temperature, low water temperature and low ph. Rapid changes in temperature stress carp, the other hazards result in reduced growth and more chronic low level stress. Pollution is an important hazard in extensive but not intensive systems, whist lack of natural food occurs in intensive but not to the same extent in extensive systems. Predation was the 8 th highest ranked hazard. In some farms it is likely to be one of the most important welfare issues. At this, and later, life stage, predation is more likely to result in physical damage leading to a long duration of effect. Table 7: Welfare risk ranking: on growing Intensive on growing pond water oxygen content too low water temperature rapid change water flow too low / water ph too high Extensive on growing pond water temperature rapid change water oxygen content too low water flow too low / water ph too low / water ph too high The EFSA Journal (2008) 843, 19-28

20 unionised ammonia content h water ph too low pollution (sewage/industrial/agricultural run off) 4.8. Marketable fish Marketable fish are only kept in storage ponds. The hazards are very similar to ongrowers: low water oxygen, rapid change in temperature and low temperature. This is the only life stage where the top three ranked hazards all occur with low probability. Thus the highest ranked hazards collectively occur more frequently at this life stage than any other. Table 8: Welfare risk ranking: marketable fish water oxygen content too low Storage ponds water temperature rapid change / water temperature too low water flow too low / water ph too low water depth too shallow / unionised ammonia contenth 4.9. Broodstock Broodstock fish are only kept in storage ponds. The hazards are very similar to ongrowers and marketable fish: low water oxygen, rapid change in temperature and low temperature. The top ranked hazards all occurred with a very low probability. The top 3 ranked hazards all affected between 60-80% of the population; low water oxygen was highest ranked due to its higher severity score (4) compared with other hazards. Again, predation was the 8 th highest ranked hazard. In some farms it is likely to be one of the most important welfare issues. Table 9: Welfare risk ranking: broodstock Broodstock ponds water oxygen content too low water temperature rapid change / water temperature too low / water ph too high water flow too low / water temperature too high The EFSA Journal (2008) 843, 20-28

21 4.10. Uncertainty All the highest ranking hazards had an uncertainty score of low or medium. Medium levels of uncertainty were for suspended solids (eggs, yolk sac fry) water ph (marketable, broodstock), dissolved oxygen (yolk sac fry), water flow (over-wintering, on-growers, marketable). Uncertainty was scored based on available information. For all hazards considerable variation will exist between farms, regions and over time. This has been captured to some extent by the ranges represented by each score; however, this has not been quantified (using confidence limits) in the final risk score. When assessing the risk scores, they should be viewed as the median value with a high standard deviation Mortality Low oxygen is the most important cause of mortality, having a high score (>3) in every life stage. Low water flow is an important cause of mortality in the later life stages. This is due to the associated reduction in available oxygen. Three hazards cause high levels of mortality (score >3) for yolk sac fry and on-growers. Of the selected diseases assessed, white spot was noted as an important cause of mortality for yolk sac and free-swimming fry. The EFSA Journal (2008) 843, 21-28

22 Table 10: Mortality scores >4 and 5 for the top 6 ranked hazards for each life stage. Hazard Life stage Handling Low O 2 Fertilised eggs/embryo 5 White spot ph Low water flow Pollution Unionise d ammonia Yolk sac fry 4d 5 5a Free swimming fry 5 5b Nursed fry 4 Fingerling 1 5 Over-wintering carp 4 4 On-growers c Marketable fish 4 4 Broodstock 4 a Dubish ponds, b nursing ponds, c intensive on-growing ponds, d tank/trough 1 predation is also an important cause of mortality General discussion It is worth noting that the hazards were not distinguished by their duration of effect which generally was the same for all hazards within each life stage. The other main trend was that highly ranked risks generally affected a high proportion ( 60%) of the population and exerted severe effects (scores 3). However, the probability of occurrence was generally extremely low or very low. A few water quality parameters occurred consistently across life stages: high or low water temperature (or rapid temperature change), low water flow, low water oxygen, high or low ph. These hazards occur relatively infrequently (extremely or very low frequency), however, when they do occur the impact is severe and affects a high proportion of the population. The risk assessment cannot assess interactions between hazards. Environmental and in particular climatic conditions may simultaneously cause more than one hazard. It is possible that the resultant impact of one or more hazards, occurring at the same time, is synergistic. Oxygen paradoxically appears as an important welfare hazard in the risk assessment, although it is usually commonly accepted that carp are tolerant to low water oxygen concentration (as low as 0.9 mg/l). However, welfare issues arise before lethal limits are reached. Also, severe oxygen shortage (e.g. collapse of algal blooms) was identified as major welfare issues. Apart from water quality issues, food shortage, disease and handling featured as highly ranked hazards. White spot was an important hazard for yolk sac fry in Dubish ponds but The EFSA Journal (2008) 843, 22-28

23 not other production systems. However, both white spot and Saprolengia were important at the next life stage (free living fry) in all 3 systems. Diseases did not rank highly for the older life stages. Handling only ranked in the top 6 hazards for yolk sac fry raised in tanks or troughs. Broodstock are handled for purposes of reproduction but the duration of the effect of handling is short-lived, resulting in a low score compared with other hazards. Long term food shortage was an issue at the fry and fingerling stages Risk mitigation / Recommendations Monitoring water quality and the capacity to take remedial action would improve welfare in all life stages. In the early life stages, production in Dubish ponds may be less amenable to rapid and effective intervention compared with other production systems. The farmer s ability to mitigate environmental factors affecting many water quality and temperature hazards is limited in most carp production systems. The most important hazards occur relatively infrequently (very or extremely low frequency) and for short periods. This reduces the intervention opportunities for aquaculturists as by the time the hazard has been noted, the damage may have occurred. Reducing the impact of these hazards probably depends on developing systems and management strategies that are less susceptible to environmental and climatic changes. As an example, high levels of stocking will clearly exacerbate the impact of adverse climatic conditions causing low levels of dissolved oxygen or high levels of unionised ammonia. Of the hazards that can be described as management related only shortage of feed (during fry and fingerling stages) and handling, featured as highly ranked risks. Training and adoption of good codes of practice can reduce the impact of handling on the welfare of carp. Production systems which result, even relatively infrequently, in food shortages may be considered sub-optimal from a welfare point of view. Most carp production relies on natural productivity for some of the life stages. It is therefore inevitable that potentially, more vulnerability to shortages of feed exist compared with other types of finfish production. This is especially true for the early life stages of fish. Commercially available diets are either expensive and/or unsuitable for extensive carp farming. Pond preparation and the creation of optimal conditions for the development of natural food items are therefore vital. The design and construction of carp farms (location, size of pond, etc.) and management regime (e.g. stocking rate) should always consider continuous adequate feed supply a priority. The EFSA Journal (2008) 843, 23-28

24 CONCLUSIONS AND RECOMMENDATIONS Overall, common carp is a domesticated species that well adapted to the husbandry systems within which it is reared. A review of environmental conditions and factors that may affect welfare of common carp, Cyprinus carpio, is given in the different sections of this report. It is important however to realise that the environmental conditions are always defined by a range of interrelated factors. While each specific variable is described separately, there are very few occasions in reality where only a single factor is involved in any fish welfare issue relating to environmental conditions. For this reason, only ranges of acceptable levels for the various factors can be given and always these should be considered in the context of the other variables involved. From this review, the following conclusions and recommendations for specific hazards were drawn. Conclusions 1. Over-stimulation of eggs and yolk sac fry with excessive light will result in smaller larvae that may have lower survival rates; compared with other hazards over-stimulation was not ranked as an important cause of mortality. In carp husbandry systems, natural light is normally used and therefore light levels seldom cause problems. 2. There are no particular water flow requirements for carp under farming conditions, except for eggs and fry. Cessation of water flow helps hatching. Excessive water flows may cause crowding of fry and wasted use of energy reserves leading to starvation. Too low water flow was found in the risk assessment to be a more highly ranked hazard (causing hypoxia) in early life stages. 3. The risk assessment scoring found low oxygen also to be an important cause of mortality at all life stages; but low oxygen levels are most important in the early stages. Fry is a particularly sensitive life stage to low but also high oxygen levels. Low levels of oxygen for extended periods can lead to poor welfare. 4. Eggs exposed to levels of gas supersaturation can lead to long term effects on surviving individuals. Supersaturation of dissolved gases may lead to gas bubble formation inside the larvae causing disruption of swimming activity. 5. The physoclistous swimbladder and auditory system of carp may render them particularly vulnerable to excessive noise and vibrations. However data on the level and significance of susceptibility are not available. 6. Carp are generally capable of surviving in waters of low oxygen levels, except in the first few months of the life cycle when fry are more sensitive. However, in terms of welfare, the results of the risk assessment found low oxygen to be the most important or second most important hazard for all life stages. In ponds, occasionally severe oxygen depletion associated with collapse of algal blooms in late summer at high temperatures can affect welfare of carp. The EFSA Journal (2008) 843, 24-28

25 7. Carp can survive across a wide temperature range (from ~2 C to > 36 C) by adjustment of their level of activity. Carp larvae are however very susceptible to temperature fluctuations: temperatures high in excess of few degrees would lead to increased rates of body deformities. Rapid temperature change (close to 3 degrees per hour) rather than absolute limits is normally a significant welfare issue for carp fry. Rapid temperature change was found in the risk assessment to be an important hazard for yolk and nursed fry and also fingerlings. 8. During incubation, high water ph can lead to incomplete embryonic development and deformities and was found in the risk assessment to be an important hazard. Carp larvae are particularly sensitive to acid stress, though it was not generally highly ranked in the risk assessment. In later life stages, water ph per se has little importance in carp husbandry, it is only important in terms of its influence on other hazards (e.g. ammonia) should they be present. 9. Carp are not affected by suspended solids level except at the very high concentrations that may occur during harvesting. High suspended solids can also suffocate eggs and yolk sac fry (it was the third highest ranked hazard for these life stages). 10. Unionised ammonia can be a serious welfare issue under conditions of intensive photosynthesis such as following collapse of algal blooms. This was reflected in the risk assessment tables where unionised ammonia was highly ranked in nearly all life stages. 11. In the present carp culture systems in Europe, tank and pond design has been found related to some welfare issues as following: water temperature (most stages), suspended solids (most stages), swim bladder inflation (larvae), impaired swimming ability and poor health and slow growth rates. 12. With regards to substrate and pond bottom, unless ponds are managed carefully, anoxic layers producing toxic metabolites can develop. 13. Algal blooms can be a significant welfare risk because of their effect on ph, and because the algae may themselves be toxic to the fish; in addition, the collapse of the bloom may cause severe and acute anoxia. The results of the risk assessment indicated that algal blooms were most important during the on-growing stage. At latest stages, the hazard was considered to be less severe and to occur less frequently. 14. Carp husbandry systems in Europe allow normal social interactions between fish, and fish species in the case of polyculture. 15. Predation is a serious welfare issue particularly significant in the farm pond environment where predators such as cormorants can injure fish and induce significant stress manifested by behavioural modifications including reduction in feeding. 16. Stocking levels depend on the nature and condition of the pond. Traditionally ongrowers are stocked at a biomass of about 300 kg/ha. However, carp are shoaling fish and this determines their own local biomass level, which has been found to have no welfare implications. The EFSA Journal (2008) 843, 25-28

26 17. Carp generally feed on natural food. Above certain densities they receive supplementation with a correctly balanced feed for a fish that is already feeding on natural food. Shortage of natural food was identified as a welfare issue for fry and fingerlings. Stocking fry into ponds with insufficient supplies of suitable food will result in low survival rates, poor growth and significant deformities. Food supply is the main factor governing appropriate stocking density. This was reflected in the risk assessment results: a shortage of natural food was the highest ranked hazard for the free and nursed fry stage. 18. Diseases are one of the major welfare issues in all fish husbandry. In the case of carp it is particularly related to environment. Most carp pathogens are facultative pathogens present in the environment. Those diseases with chronic, often sub clinical effects are often of greatest welfare significance. In the case of the more acute conditions, control or treatment measures may have significant welfare impact in their own right. 19. Currently, very few of the treatments which are effective can be used due to the fact that these veterinary medicinal products are not authorised for use in carp. Absence of medicinal products may pose welfare problems. In practice treatment using unauthorised veterinary medicinal products may in itself represent a welfare concern. 20. The risk assessment scored three diseases selected to be used as working examples. These hazards affected mainly the earlier life stages (fry) and their welfare significance varied between production systems. 21. For yolk sac fry, risk assessment highlighted a difference between tanks/troughs and Dubish ponds, with white spot disease (Ichthyophthirius multifiliis) being the highest ranked risk in Dubish ponds. 22. Overall, the husbandry systems for each life stage did not differ considerably in their risk ranking. 23. The nets used during the harvest process induce stress and may also increase the risk of physical trauma and damage to the fish skin. Recommendations 1. For eggs and yolk sac fry, light levels should be kept low to avoid over-stimulation leading to exhaustion of endogenous reserves. 2. The water flow for egg incubation should not exceed 1.5 l/min during the first hours of development and 3 litres per min thereafter. 3. For fry, excessive water flows should be avoided to prevent crowding of and wasted use of energy reserves leading to starvation. 4. Carp larvae are particularly sensitive life stages to low and high oxygen levels and levels should be maintained between 6 and 8 mg/l during this phase of culture. 5. Eggs and larvae should not be exposed to levels of gas supersaturation, which can lead to short and long term effects on individuals, including swimming capacity. The EFSA Journal (2008) 843, 26-28

27 6. Carp larvae are very susceptible to temperature fluctuations; fluctuations over 1 C should be avoided during transfer from incubation system to hatching system. 7. During incubation, water ph should be maintained between 6.0 and The water supply to the hatchery water should be filtered to limit suspended solids as high suspended solids can suffocate eggs and embryos. This will also limit entry of predatory invertebrates. 9. Unionised ammonia can be a serious welfare issue under conditions of intensive photosynthesis such as following collapse of algal blooms and great care and understanding are required in levels of fertiliser utilised in pond management to avoid this hazard. 10. Over-wintering ponds should be properly designed and sufficiently deep for the coldest weather. 11. Catch pits in harvest ponds should be carefully designed to minimise the suspended solids problems. 12. Harvesting the ponds should occur when water temperatures have dropped below 14 C, when carp have a significantly reduced metabolic activity and their requirement for oxygen is diminished. 13. During harvesting operations, efforts should be made to maintain the fish in water of sufficient oxygen content, either by removing the fish as quickly as possible or by introducing fresh, oxygen-rich water into the catchpit. Efforts should be made to crowd fish carefully to reduce the possible effect of net damage. 14. For larvae, tank design should enable swim bladder to fill with air in order to prevent its incomplete development, and subsequent impaired swimming ability and poor health and slow growth rates. 15. Grow-out ponds should be carefully managed to prevent anoxic layers producing toxic metabolites can develop. 16. Algal blooms can be a significant welfare risk at on-growing stage because of their effect on ph, oxygen, and possible direct toxicity. The levels of algae in ponds should be monitored and maintained at levels to avoid the development of blooms and the harmful effects following bloom collapse. On farm reliable emergency backup is also recommended. 17. When stocking ponds, there should be minimal disturbance of the fish and sudden changes in temperature should be avoided. During the early rearing, stocking levels should be matched to the plankton availability. 18. Larval feed should contain 40-50% protein. The size of food particles is extremely important since first feeding fry can consume food of only a few hundred microns in size. In the later part of the nursing period fry may consume feed up to 1 mm in size. The quantity of artificial feed is to be defined based on the abundance of zooplankton, survival rate and age of the fry. Initially fry require kg food/ fish. 19. Ponds populated mostly or only with herbivorous species require 20-40% less fertilisers than common carp in monoculture since the herbivorous fish feed on water plants and recycle nutrients back into the pond after digestion. The EFSA Journal (2008) 843, 27-28

28 20. Fry require good quality supplementary feed with a digestible crude protein content of 25-30%. Mixtures of cereals or legumes, or industrial by-products are used. If the natural feed (protein) supply runs out during the growing season a high protein diet based on fish or meat meal should be given. 21. Larvae should never be removed from the water. 22. Research should determine if genetic selection could affect traits that have a negative welfare impact. 23. Disease is one of the major welfare issues in all fish husbandry. Good husbandry should be the major means of disease control. 24. Rearing ponds for carp fry should range between 500 and m 2 in size with an average depth of m and sheltered from excessive wind. 25. Storage ponds should be around 2 m deep in order to reduce the effect of changes in ambient air temperatures. Shape and slope of the bottom and the design of the catch pit should ensure rapid and efficient fish crowding. Concrete bottoms should be avoided as they may result in traumatic skin lesions. When a pond is partially emptied, suitable equipment should be used to prevent physical damage to the remaining stocks as well as to the harvested fish. 26. Over-wintering carp ponds should be m deep. They should have a soft bottom with a low proportion of organic matter. The pond should be supplied with appropriate inflow of clean well aerated water and it is important that overwintering ponds are sufficiently deep for the coldest weather. 27. Disinfection and husbandry discipline are key component of biosecurity. A particular attention should be given to transportation equipment both before and after transportation of fish. 28. In view of the risks associated with the movement of live fish, including Koi carp, improvement in biosecurity is needed, at national and farm level. There is a need for training and establishment of robust biosecurity arrangements that will be both applied and monitored. 29. Vaccines have made a significant contribution to controlling serious infectious diseases of fish. Future research on effective vaccination of carp against major infectious diseases is recommended as a means of improving carp welfare in this regard. 30. There is a need for authorised veterinary medicinal products for carp disease treatments. The EFSA Journal (2008) 843, 28-28

29 The EFSA Journal (2008) Annex I, 1-81 SCIENTIFIC REPORT ON ANIMAL WELFARE ASPECTS OF HUSBANDRY SYSTEMS FOR FARMED COMMON CARP (Question N EFSA-Q ) Issued on the 22 nd of October 2008 European Food Safety Authority, 2008

30 WORKING GROUP MEMBERS The members of the Working Group responsible for the preparation of this report were: Ronald Roberts (Chairman, Member of the Animal Health and Welfare Panel), Edmund Peeler (Risk Assessor), Zdenek Adamek, Alan Henshaw, Zsigmond Jeney, Maciej Pilarczyk, Rodney Wootten and Felicity Huntingford. ACKNOWLEDGEMENTS In addition the Scientific Panel on Animal Health and Welfare wishes to thank Flavio Corsin for his contribution to the scientific review of this report. PANEL MEMBERS This scientific report was peer reviewed by the Members of the Scientific Panel for Animal Health and Welfare (AHAW) of the European Food Safety Authority. The scientific report was used as the basis for the scientific opinion adopted on this matter. The members of the AHAW Scientific Panel were: Bo Algers, Harry J. Blokhuis, Donald M. Broom, Patrizia Costa, Mariano Domingo, Mathias Greiner, Daniel Guémené, Jörg Hartung, Per Have, Frank Koenen, Christine Müller-Graf, David B. Morton, Albert Osterhaus, Dirk U. Pfeiffer, Ronald Roberts, Moez Sanaa, Mo Salman, J. Michael Sharp, Philippe Vannier, Martin Wierup. The EFSA Journal (2008) Annex I, 2-81

31 SUMMARY The scientific report on the animal welfare aspects of husbandry systems for farmed common carp constitutes the background document to the opinion adopted by the Panel on Animal Health and Welfare on the 22 nd of October The common carp (Cyprinus carpio, Linnaeus 1758), which is by far the species farmed in largest numbers, is a domesticated species that has well adapted to the husbandry systems within which it is reared. In Europe, only two major production systems (monoculture of carp and polyculture of carp) are commonly practised. There are numerous combinations of polyculture with common carp production. Since the species involved are all cyprinids and occupy only slightly different ecological niches in the pond system, they were subjected to the same risk and hazard assessments as carp in monoculture. Consequently, for the purpose of risk assessment, polyculture was considered as an intensive monoculture production system. The various life stages of carp considered are: fertilised eggs and embryos, yolk sac fry, free swimming fry, nursed fry, fingerling, overwintering carp, on-growers, marketable fish, and broodstock. A review of environmental conditions and factors that were identified as possibly affecting the welfare of common carp, Cyprinus carpio, at different life stages has been conducted. These factors are grouped as: abiotic and biotic factors (including behavioural interactions), food and feeding, husbandry and management, genetics, and the impact of disease and disease control measures. It is however important to realise that the environmental conditions are always defined by a range of inter-related factors. While each specific variable is described separately, there are very few occasions in reality where only a single factor is involved in any fish welfare issue relating to environmental conditions. For this reason, only ranges of acceptable levels for the various factors can be given and these should always be considered in the context of the other variables involved. Key words: carp, animal welfare, risk assessment, fish farming, husbandry system, aquaculture, environmental conditions, biotic factors, feeding, husbandry, disease. The EFSA Journal (2008) Annex I, 3-81

32 TABLE OF CONTENTS Working Group Members... 2 Acknowledgements... 2 Panel Members... 2 Summary... 3 Table of Contents... 4 List of tables... 6 Background as provided by european commission... 7 Terms of reference as provided by european commission... 7 Assessment Scope and objectives of the report Taxonomy of carp Biology of common carp Overview of carp production systems in Europe Carp production in Europe Main production systems Monoculture of carp Polyculture of carp Culture of carp integrated with other agricultural activities Life stages of carp in production systems Factors affecting the welfare of carp Abiotic factors Light period and intensity Noise and vibration Water flow Water oxygen content Total dissolved gases Water temperature Water ph Suspended solids Ammonia content Pond size and morphology Substrate of ponds Environmental pollutants Environmental conditions biotic factors Algal blooms Behavioural interactions Predation Stocking density Food and feeding Husbandry and management Stocking Handling and harvesting Handling of broodstock Separation of Sexes Anaesthesia Hypophyseal hormone treatment Stripping and egg fertilization On-farm movements Sorting and Grading Monitoring Staff training on welfare Genetics Impact of diseases on welfare The EFSA Journal (2008) Annex I, 4-81

33 Parasitic diseases: White Spot (Ichthyophthirius multifiliis) disease Fungal diseases: saprolegniasis Bacterial diseases: motile Aeromonas septicaemia Viral diseases: spring viraemia of carp Disease control measures Biosecurity Monitoring mortalities / survival rates Drug usage Vaccination Methods of vaccination Welfare and vaccination in fish Risk assessment approach to welfare of common carp Introduction Steps of risk assessment Hazard identification Hazard characterization Exposure Assessment Uncertainty Scoring process Risk characterization Discussion Introduction Stage specific discussion Eggs Yolk sac fry Free living fry Nursed fry Fingerlings Over-wintering On-growers Marketable fish Broodstock Uncertainty Mortality General discussion Risk mitigation References Appendix. Carp farming system Glossary / Abbreviations The EFSA Journal (2008) Annex I, 5-81

34 LIST OF TABLES Table 1. List of farmed species of the carp family (Cyprinidae)... 9 Table 2. Life stages in different carp production systems Table 3: Severity of adverse effect Table 4: Likelihood of effect (proportion of population affected) Table 5: Frequency of exposure Table 6: Uncertainty score Table 7: Welfare risk ranking: eggs Table 8: Welfare risk ranking: yolk sac fry Table 9: Welfare risk ranking: free living fry Table 10: Welfare risk ranking: nursed fry/nursing Table 11: Welfare risk ranking: fingerling Table 12: Welfare risk ranking: Over wintering Table 13: Welfare risk ranking: on growing Table 14: Welfare risk ranking: marketable fish Table 15: Welfare risk ranking: broodstock Table 16: Mortality scores >4 and 5 for the top 6 ranked hazards for each life stage The EFSA Journal (2008) Annex I, 6-81

35 BACKGROUND AS PROVIDED BY EUROPEAN COMMISSION Council Directive 98/58/EC concerning the protection of animals kept for farming purposes lays down minimum standards for the protection of animals bred or kept for farming purposes, including fish. In recent years growing scientific evidence has accumulated on the sentience of fish and the Council of Europe has in 2005 issued a recommendation on the welfare of farmed fish 1. Upon requests from the Commission, EFSA has already issued scientific opinions which consider the transport 2 and stunning-killing 3 of farmed fish. TERMS OF REFERENCE AS PROVIDED BY EUROPEAN COMMISSION In view of this and in order to receive an overview of the latest scientific developments in this area the Commission requests EFSA to issue a scientific opinion on the animal welfare aspects of husbandry systems for farmed fish. When relevant, animal health and food safety aspects should also be taken into account 4. This scientific opinion should consider the main fish species farmed in the EU, including Atlantic salmon, gilthead sea bream, sea bass, rainbow trout, carp and European eel and aspects of husbandry systems such as water quality, stocking density, feeding, environmental structure and social behaviour. Due to the great diversity of species it was proposed that separate scientific opinions on species or sets of similar species would be more adequate and effective. It was agreed to subdivide the initial mandate into 5 different questions in relation to Atlantic salmon, trout species, carp, sea bass and gilthead sea bream, and in relation to European eel. 1 Recommendation concerning farmed fish adopted by the Standing Committee of the European Convention for the protection of animals kept for farming purposes on 5 December Opinion adopted by the AHAW Panel related to the welfare of animals during transport -30 March Opinion of the AHAW Panel related to welfare aspects of the main systems of stunning and killing the main commercial species of animals- 15 June Food Safety aspects of fish welfare are addressed by a Scientific Opinion of the BIOHAZ Panel ( Food Safety aspects of Animal welfare aspects of husbandry systems for farmed fish, Question N EFSA-Q ). The EFSA Journal (2008) Annex I, 7-81

36 ASSESSMENT 1. Scope and objectives of the report In Europe, the common carp (Cyprinus carpio, Linnaeus 1758) is by far the carp species farmed in largest numbers. Therefore, it is used as a basis for this report. Variations in the methods for its husbandry are presented where they occur, although rather limited differences exist among the farming systems in Europe. Although common carp has been domesticated for several thousands years, it is currently farmed in Europe under husbandry systems where issues of welfare have not to date been comprehensively analysed. The welfare aspects of carp culture is in many ways less than adequately described in the scientific literature and so, expert opinion and industrial experience have had to be referred to where necessary. The various areas within the production systems where specific welfare risk might be considered to exist have been identified. These risks were analysed in relation to the different life stages and production systems based on available scientific literature and expert practical experience. The welfare risks, which have been identified as a result of the literature review, have been subjected to a semi-quantitative risk assessment. The objective of this report is to highlight how husbandry systems may increase the likelihood of negative effects on the welfare of common carp. 2. Taxonomy of carp The order Cypriniformes comprises 6 families of which Cyprinidae is one. The family Cyprinidae has at least 1700 species; this makes the family the most important in numbers of species of all freshwater teleosts (Howes, 1991). The Common Carp (Cyprinus carpio, Linnaeus 1758) is one of the most widespread members of the Cyprinid family and is present (due mainly to human activity) throughout continental Europe, Australasia, Africa, India and the Americas. All of the species included in Table 1 are farmed in Europe, sometimes for food, sometimes for restocking, or angling, and some for sale as ornamental species (e.g. Koi carp). In Europe, however, as in Asia, the common carp, Cyprinus carpio, is by far the most widely cultured carp species for all of the above purposes. In both numbers of animals farmed and in terms of economic value, it is the most important species. Because of its economic value common carp is also the species about which the largest volume of scientific, husbandry and, in a lesser extend, welfare information is available and so this report will focus specifically on welfare aspects of husbandry systems of common carp. Many of the features of carp husbandry, however, are common to the other species as well, indeed they are often grown together in polyculture (see glossary) and so the data given will in many ways be relevant also to the other carp species. The EFSA Journal (2008) Annex I, 8-81

37 Table 1. List of farmed species of the carp family (Cyprinidae) 5 Species Cyprinus carpio Linnaeus 1758 Ctenopharyngodon idella (Valenciennes 1844) Hypophthalmichthys molitrix (Linnaeus 1758) Aristhichthys nobilis (Richardson 1845) Tinca tinca (Linnaeus 1758) Abramis brama (Linnaeus 1758) Carassius carassius (Linnaeus 1758) Carassius auratus (Linnaeus 1758) Barbus barbus (Linnaeus 1758) Leuciscus leuciscus (Linnaeus 1758) Leuciscus cephalus (Linnaeus 1758) Leuciscus idus (Linnaeus 1758) Rutilus rutilus (Linnaeus 1758) Scardinius erythrophthalmus (Linnaeus 1758) Cyprinus carpio Var Koi (Linnaeus 1758) Vimba vimba (Linnaeus 1758) Mylopharyngodon piceus (Richardson 1846) Purpose of production Common name Food Restocking Ornamental Production importance (1-5) 1 less important to 5 most Carp X X - 5 Grass Carp X X X 4 Silver Carp X Big Head Carp X Tench X X X 3 Common Bream Crucian Carp X X - 1? X X 2 Goldfish - - X 3 Barbel - X - 1 Dace - X - 1 Chub - X - 1 Ide - X X 1 Roach - X - 1 Rudd - X X 1 Koi Carp - - X 3 Vimba - X - Black Carp X - - Data not available Data not available The common carp is the oldest cultured and most domesticated fish in the world; having been farmed for about 4000 years in China and for several hundred years in Europe (Wohlfart, 5 This table has been prepared by the working group in the absence of a comprehensive published document on the subject. The following references have been used: Gaudet 1967, and Poncin & Phillipart The EFSA Journal (2008) Annex I, 9-81

38 1984). The common carp is believed to have originated in Central Eurasia (Balon, 1974) and may be divided into several sub-species or races, namely the European-Transcaucasian, the Amur-Chinese and the South-east Asian carp, reflecting the different centres of domestication. Numerous varieties and sub-varieties of strains of carp are available in South- East Asia (including Japan), the Russian subcontinent and Eastern and Central Europe that are cultured for food and as ornamental fish. 3. Biology of common carp The ecological spectrum of carp is wide. Carp occur naturally in summer-warm lakes and slowly flowing rivers. Carp are rarely found in clear, cool, swift-flowing streams. They prefer muddy areas where they search for food organisms (Steffens, 1975; Hepher and Pruginin, 1981; Horvath et al., 1992). Common carp demonstrate cyclic growth related to the annual cycle of temperature. In spring they emerge from a state of virtual hibernation to commence a rapidly increasing feeding level. They grow best in waters where the temperature exceeds 20 C for at least two months of the year. They can tolerate temperatures above 30 C for short periods. Such temperatures, at the height of summer can lead to very rapid growth rates. Once temperatures fall, however, common carp cease feeding and re-enter a state of torpor during which energy requirements are limited and tissues are maintained as far as possible by metabolic conservation. Carp can tolerate winter temperatures below 2 C. Carp usually do not migrate to long distances for food or reproduction. They usually move in small groups, searching for food or suitable spawning areas. Sometimes they may move on longer distances, but these movements are related to feeding activities. Carp are omnivorous fish with a strong tendency to eat animal food, such as benthic animals (Chironomidae, Oligochaeta) and planktonic crustaceans (Cladocera, Copepoda). Carp also ingest detritus, decaying and green plants or parts of them, such as like leaves and seeds (Alikhuni, 1966; Sarig, 1966; Adamek et al., 2003). Zooplankton consumption is dominant in one-year-old fish. Older carp prefer benthic food organisms (Spataru et al., 1980), but are still able to feed on crustaceo-plankton if available. The quantity and quality of natural food organisms depends basically on the stocking density of fish and, in the case of polycultureoperated farms, on the species ratio in carp fish ponds. Since fish overgraze the natural food organisms when stocked above a certain standing crop (Hepher and Pruginin, 1981), at high stocking densities protein rich pellets are needed to satisfy their feed requirement. In Central Europe, carp reach maturity in their third to fourth (male) or fourth to fifth (female) year of life. However in warmer climates, for example in the Mediterranean region, carp growth may be much faster and maturation may appear earlier. For European carp strains, the main triggering factors for spawning in the wild are: presence fish of the opposite sex, appropriate temperature, increasing water level and availability of an appropriate spawning substrate. Carp normally spawn in late spring on aquatic vegetation, as a phytophilous (see glossary) fish species (Horvath et al., 1992). Besides submerged aquatic plants, carp often lay their eggs on flooded grass beds during late spring flooding events. Common carp eggs are sticky. Once released from the female and fertilised, the eggs attach themselves to various substrates. Carp spawning starts when water temperatures exceed C. At water temperatures below this range, and in water warmer than 26 C, natural spawning stops (however, there are carp strains adapted to low water temperatures, the spawning of these strains may start at C). The mating groups comprise usually one or two females and several males. The male fish follow the female, and both swim near to the surface in shallow waters close to the edge or The EFSA Journal (2008) Annex I, 10-81

39 bank of the water body. The male pushes its body to the female followed by egg release. Carp do not guard the eggs (Balon, 1995). Wild carp are partial spawners, two to three portions of eggs being released at about 2 week intervals (Balon, 1995; Adamek, 1998). The female produces between 80,000 and 1,500,000 eggs depending on the size of the fish, and relative fecundity ranges between 150,000 and 300,000 eggs per kg (Steffens, 1975; Brylińska, 2000). The period of time between fertilisation and hatching is about degree-days (see glossary) and the fry emerge to utilize their food supply in the yolk-sac as they gradually develop functioning gills and digestive tract. Fry start to feed on rotifers 3-5 days after hatching. As gut extends into four and finally eight folds, carp switch from rotifers into Copepoda and Cladocera to feed intensively on Chironomidae when reaching body length of about 4-5 cm. Once fully weaned carp are omnivorous and diet will include wide spectrum of feed including planktonic and benthic animals such as Chironomidae, Ephemeroptera, Oligochaeta, Gastropoda and Hirudinea. Under natural conditions, carp rarely feeds on plant matter, but can ingest seeds or small fruits found in a pond (Brylińska, 2000). Accidents of predation or cannibalism are very seldom, but have been reported under extremely poor feeding conditions (Wolny, 1974). Common carp is a long-lived species achieving age of 45 years and weight of about 30 kg. 4. Overview of carp production systems in Europe 4.1. Carp production in Europe The production of carp dates back several thousand years, with most of the cultured species originating from Asia. The four most important species of cyprinids, i.e. the common carp (Cyprinus carpio), the silver carp (Hypophthalmichthys molitrix), the bighead carp (Hypophthalmichthys nobilis), and the grass carp (Ctenopharyngodon idella). Cyprinidae form the dominant group of species in terms of production, accounting for 30% of the global aquaculture production and 69% of the freshwater aquaculture production (FAO, 2006). According to the FAO statistics, production of farmed common carp was 13% of the total global freshwater aquaculture production in Common carp production has increased by an average global rate of 10.4% over the past decade. The vast majority of the production originates from Asia (97% - with China claiming 70% of the production) with the majority of the production consumed domestically. In Europe, production of common carp has declined sharply, between 1990 and 2004, reflecting socio-economical changes in Central and Eastern Europe. Carp production in Europe is currently of about 225,000 metric tons (mt) and 90% of this is produced by aquaculture. The dominant technology is carp-based polyculture production in ponds. As mentioned above, considerable decline in production occurred after the changes in Central Eastern Europe in the early 1990s, followed by a slow but steady growth. Aquaculture of carp is important not only as a food supply, but also for restocking and recreational fishing. The fish processing industry is relatively undeveloped for carp, although there have been positive changes recently. There are very few intensive systems in the region despite existing technology (see section 4.2). The main common carp-producing countries, and their share of the total production, in 2005, were: Poland (26%), the Czech Republic (25%), Hungary (14%) and Germany (17%). In these countries, inland aquaculture is heavily based on cyprinids, which contribute to about 70% of the total production. Fish production is an option in areas that are unsuitable for other types of agricultural production. Although the carp sector has recently had marketing The EFSA Journal (2008) Annex I, 11-81

40 difficulties, the creation of new ponds and the expansion of existing ones are options. Due to relatively high investment costs, it is difficult to build new pond culture farms. The only option for increasing the area of production is to reconstruct abandoned ponds that are not too degraded. European temperatures dictate that production of table-size fish ( kg) in pond culture takes three to four years. The fish are harvested at the end of each season and restocked after overwintering in storage ponds. In semi-intensive ponds, the fish are fed with plankton (enhanced with manure application) and complementary feeding with grains. In extensive ponds, there is no manuring or feeding. In extensive aquaculture, yields are usually expressed in volume of production per surface unit. The average yield varies between 600 and 1500 kg/ha, depending on the level of intensity (Horváth and Urbányi, 2000). Interest in organic production of carp in ponds is increasing rapidly, but consumers are generally not willing to pay higher prices that result from the higher average costs, extra inputs, and losses in yield that accompany organic production. The major technical obstacle to organic production is obtaining organic feedstuffs. Because there is no common legislation/control of organic carp production, it creates uncertainty among producers and consumers. Carp will probably remain the dominant species produced in Central and Eastern Europe, due to traditions and a relatively constant demand. Nevertheless, the proportion of other (especially higher-value) species produced is likely to increase. Marketing, breeding, and technological conditions do not prevent the production of other species, so diversification is feasible. Innovation and the willingness of producers to diversify are expected to be the key factors of this issue in the future. Diversification involves changing from current monoculture to polyculture systems by combining finfish, shellfish, and algal culture to reduce net effluent levels and improve spatial productivity per unit area. The three main areas of mechanization in pond farming are aeration, feeding, and harvesting. Aeration is generally part of the technology for intensive ponds, where built-in equipment provides fish with a suitable amount of oxygen throughout the breeding season according to the oxygen content of the water. Feeding boats are generally used in ponds to apply supplementary feeding. Intensification of production, however, requires the use of special feeders. Feeding is a crucial point in carp farming, because it can substantially influence the efficiency of production, although intensive feeding does not necessarily result in increased efficiency. Harvesting is conventionally mechanized with the use of equipment such as fish collector pulleys and cranes. The use of modern machinery to separate fish by size (grading) is becoming more important. New and greatly modified pond systems and technologies were the result of requirements for higher-quality products and for protecting the environment and water resources. As the problem of water conservation and use is given increasing priority, special technologies (no drainage for years) are expected to appear. There are other methods for saving water, including water circulation within a pond system or among ponds, e.g., using extensive ponds to purify effluents from intensive ponds (which are rich in nutrients). Environmental issues are not crucial constraints for carp production in Europe. They constitute a risk for intensive and monoculture-type farming that can be mitigated by diversification along with more extensive production. Pond culture of carp is considered to be an extensive, sustainable farming and thus, unlike other types of aquaculture, it has a very limited negative impact on the environment. Indeed, extensive carp aquaculture can help to improve environmental protection and restoration in many ways while exploiting the natural resources of water bodies. Developing extensive farming is a way to associate an economic The EFSA Journal (2008) Annex I, 12-81

41 activity with the conservation/development of wetlands. Unfortunately, their dependence on natural processes also represents a limit to their productivity, implying low compatibility with intense economic activity (see also ) Main production systems Three main production systems of common carp can be differentiated as: i) monoculture of carp, ii) polyculture of carp, and iii) integrated carp culture with other agricultural activities. Here we give a short description of these three systems; however it should be emphasized that during recent years only carp monoculture and carp polyculture is practised on a wide base in Europe. Multifunctional carp farming and organic carp farming have a perspective for becoming separate production systems in future according to recent studies (Szucs et al., 2007). A schematic representation of carp farming is provided as an Annex to this report Monoculture of carp In Northern areas of Europe (e.g. Poland), the monoculture of common carp is more characteristic, because silver and bighead carp are less tolerant of the colder weather. Common carp are cultured primarily in earthen ponds. The culture intensity ranges from extensive (low stocking densities, with no supplemented feeding or fertilisation) to relatively highly intensive (high stocking density, feeding complete diets, mechanical aeration, management of water quality, including phytoplankton blooms). Extensive monoculture is the traditional method in Europe and is carried out in large ponds which may be up to several hundred hectares in size. In western and central Europe this method requires three growing seasons to produce a marketable fish of kg and in Eastern Europe two growing seasons are required to produce a market fish of kg. Natural production, based only on pond productivity is low, from kg/ha/yr depending on soil conditions and water quality. Liming and mineral fertilisers increase production to kg/ha/yr, but success is very dependent on climatic and soil conditions. The type, level and frequency of inorganic fertilisation vary considerably between countries. Organic fertilisation can also be used to increase natural food but carp production is usually below 1000 kg/ha/yr and may be much less. Higher yields of up to 1500 kg/ha/yr can be obtained in a well managed system with supplemented feeding e.g. cereals at 1-3% body wt. Such feed may also serve as an organic fertiliser enhancing the bacterial detrital food chain (Olah, 1986). In Europe the stocking density of common carp depends on the level of intensification of the culture system, e.g. in the 3 rd growing season from fish/ha in unfed and unfertilised ponds to 900 fish/ha in fertilised ponds. Intensive monoculture of common carp is based upon the use of pelleted food, and vigorous aeration or flowing water, in net cages in lakes and still or flowing water ponds. Production costs are high and given the low market price of common carp intensive culture is no longer widely practised Polyculture of carp Polyculture involves the culture, in the same pond, of several fish species that feed on different natural resources and thus maximise the production potential of the pond. The EFSA Journal (2008) Annex I, 13-81

42 Polyculture in Europe expanded from the 1960s with the introduction of Chinese carp (bighead carp, silver carp, grass carp and other species) with different food habits, both to improve water quality and increase fish production. The typical polyculture consists of common carp (50% to 60%), silver and bighead carp (25% 30), and grass carp (2% 5%). The remaining stocks usually encompass pike, Esox lucius, pikeperch, Stizostedion lucioperca, and Wels catfish, Silurus glanis, and other species (e.g. tench, Tinca tinca). Stocking percentages may vary according to the prevalent weather conditions. The use of different carp species in polyculture utilises all the ecological niches available (surface, middle and bottom feeding). Moreover, the growth and yield of each carp species may be higher in polyculture than in monoculture. The autotrophic and heterotrophic levels are improved (Hepher et al., 1989). The natural production ratio of a polyculture population compared with a monoculture production of common carp was established by Horvath et al. (1984). The improvement in production due to polyculture is less marked in ponds with good natural resources. In Europe polyculture often involves only two or three species (common carp, silver and grass carp) (Horvath et al., 1984; Sharma and Olah, 1986; Olah, 1986). Other cyprinid and carnivorous species may be stocked with carp but the ratio between these other species and the carp will depend on whether the main objective of the pond production is for food fish or for restocking (Kestemont, 1993) Culture of carp integrated with other agricultural activities Integrated farming may improve the economic viability of the separate parts of the operation (Muir, 1986; Little and Muir, 1987). In aquaculture/agriculture systems integration may be direct (use of the same area for different activities), indirect (use of by-products from other activities in other areas), parallel (use of the same area at the same time), or sequential (rotation of activities in the same area). Integrated aquaculture is often associated with polyculture, and carp, because of their adaptability are almost always involved in such systems. As yet there has been little development of such systems in Europe. As mentioned earlier in this section, only two major production systems (monoculture of carp and polyculture of carp) are commonly practised in Europe. In the following sections these two production systems will be described in details and analysed from a fish welfare point of view. Although there are numerous combinations of polyculture with common carp production, since the species involved are all cyprinids and occupy slightly different ecological niches in the pond system, there are subject to the same risk and hazard as carp in the monoculture system. For risk assessment, as a simplification, carp polyculture will be considered as an intensive monoculture production system, only considering the number of individuals not their species richness Life stages of carp in production systems The different life stages of common carp that are considered in this report are summarised in Table 2, along with a brief description and comments related to different production systems. The diagram in Appendix B represents the various possible production systems used for each life stage of farmed common carp also giving an indication of the duration of each stage. The EFSA Journal (2008) Annex I, 14-81

43 The egg stage is not normally considered as a stage at which welfare issues would arise per se. However, it is recognised that hazards, which occur during incubation of eggs can influence the long term welfare of the organism such as body deformities. Carp culture does not involve wild caught fingerlings. In hatchery, the adult fish (spawners) are usually hand-stripped; eggs are fertilised and the fertilised eggs incubated in purpose made incubators (Zuger Jars or inverted bottles). These conical shaped vessels commonly have a volume averaging between 7 and 9 litres, are supplied with a controlled up-welling flow of water with a spout or outflow at the top. However, if jars are used for incubation, the eggs have to be treated to remove their stickiness. A number of techniques are used to achieve this including the use of tannin, milk, talc and proteolytic enzymes. Semi-natural egg production takes place in specially designed and prepared ponds where the adult fish are encouraged to spawn usually in response to hormone injections. This technique is commonly referred to as the Dubish method. Hatching of carp larvae usually takes place after degree days and as hatching commences, the eggs and larvae can be siphoned out into hatching troughs or removed by an overflow system. Immediately after hatching, the larvae stick to vertical surfaces using a small gland on the head. At this stage the larvae are approximately 4.8 to 5 mm long. The larvae stay in this position until such time as they have absorbed the majority of the yolk sac and they begin to inflate the swim bladder. Under normal circumstances this usually takes degree days and the larvae are now 6.0 to 7.0 mm in length (Horvath and Lukowicz, 1982). The larva inflates the swim bladder by swimming up to the water surface and taking in small amounts of air. This is done incrementally and may take a number of hours to complete. Once the swim bladder is fully inflated the larvae are able to swim normally, maintain position in the water column and able to seek external food items. After the larvae have hatched and 60 to 70 degree days have elapsed, the swim-up stage is completed and the fry begins to feed on Rotifera and Ciliates. In well prepared ponds, these invertebrates are in abundance and the fry grows quickly reaching 2.5 cm and 0.2 g in 3 to 4 weeks. Survival rates to this stage range from 40 to 80% depending on a number of factors. Nursing fry is a critical phase in carp production because it is the time that the delicate freeswimming larvae are stocked in a natural pond environment. The nursing period lasts about 4 weeks and its success is based on correct pond preparation which ensures the establishment of an abundance of natural food within the pond, and the maintenance of suitable water quality. At this stage the fry are very sensitive and it is essential to provide a good diet which leads to high survival and a satisfactory growth rate (Billard, 1999). Fingerling production starts with the stocking of fry (15-40 mm length, g weight) into ponds (Table 2). Polyculture is often used at this stage of carp production. The production of one-summer fingerlings provides the basis for market fish production. This stage therefore needs to be carefully managed to provide the required number of good quality fish at the end of their first summer. Pond fertilising and supplementary feeding are crucial and require closer attention than at other stages of the life cycle. A production season starts and finishes with harvesting and grading of fish in spring and autumn. Usually, the fish are not handled between these two events unless the population is sampled for growth rate, condition and health status. On-farm transport (from/to storage/winter ponds) is an important, unavoidable part of the production process which also has welfare implications. The EFSA Journal (2008) Annex I, 15-81

44 The process of harvesting (spring and autumn) is achieved by gradually draining the pond until the fish are crowded in a catch-pit. From here they are netted and removed either to over wintering ponds or to stock ponds prior to marketing. Overwintering ponds are designed to maintain adequate liquid water volume for carp stocks during the period of the year with ice cover of the ponds. The fish are in a state of very low metabolism. They do not feed and have very low respiratory and excretory levels. During this period, production ponds are drained, fallowed, and prepared for the coming production season. After final harvest (Table 2) marketable carp are kept in storage ponds until they are sold, normally a period of 4 to 10 weeks, at low temperature. Sexual maturation of carp is dependent on water temperature (Horvath et al., 1984). In Southern Europe carp will become sexually mature within 2-4 years. This time increase to 4-5 years in Central Europe, and 5 years or more in Northern Europe. Males generally mature one or two years earlier than females. Spawners that are spawning for the first time are usually preferred, because their eggs are easier to collect, the fish themselves adapt quickly to being kept in tanks. The general rule for raising broodstock is to select healthy fish with good physical characteristics (Horvath et al., 1984). Under proper holding conditions spawners will produce mature oocytes at 10-15% of their body weight by the autumn season. Table 2. Life stages in different carp production systems. Life stages Fertilised eggs/embryo Yolk sac fry Free swimming fry Nursed fry Description Early developmental stage of fish, after fertilising the eggs with sperm Life stage between hatching and starting to swim/feed. Life stage after starting to swim and feed to approx. 1 month Approx. 1 month of age young fish 1. Polyculture of carp with other fish species Production systems 2. Carp monoculture Eggs and sperm are collected after hormonal induction. After artificial fertilisation, the embryonic development takes place in hatching jars or trays. Hatching yolk sac fry are siphoned into larvae keeping containers, where they stick to the wall. Consumption of yolk sack. Free swimming fry will be moved to the nursing or fingerling ponds and will search for food, OR Free swimming fry will be moved into the nursing or fingerling ponds only after receiving the first food indoor. Free swimming fry will be reared in nursing ponds for approximately 1 month and will be moved to fingerling production ponds until one year age. Essential difference between system 1 and 2 Spawning by natural way in small prepared spawning ponds also known as Dubish ponds Breeders are removed from the pond. Timing for removal of breeders is mainly dependant on pond design (Dubish). Yolk sac fry will hatch from the embryo and stick against the underwater vegetation. Free swimming fry will begin feeding indoor or outdoor.. None The EFSA Journal (2008) Annex I, 16-81

45 Fingerling Juvenile fish until one year of age Free swimming fry or nursed fry will be reared in fingerling production ponds until one year of age. None Overwintering carp Carp (fingerlings, on-growers, broodstock) stocked into the overwintering ponds or left in grow-out ponds for the winter period Carp will overwinter in overwintering ponds OR Left in deep grow-out ponds None On-growers Carp until the age of two to four years Carp will be grown in production ponds until two or three summer age in polyculture with other fish species. Carp will be grown in production ponds until two or three summer age in monoculture. Carp will be grown in monoculture or in polyculture. Marketable fish Two-four yearold carp ready for human consumption Carp of the desired weight will be kept in storage ponds before leaving the farm to the market or processing. None Broodstock Mature female and male carp selected for reproduction Broodstock is grown in separate ponds. Males and females will be separated into different ponds before the reproduction season, in case of their use for artificial reproduction. None 5. Factors affecting the welfare of carp Although carp culture uses many techniques that are closely analogous to what these fish experience in the wild, fish culture systems inevitably introduce a number of stressors to the organism. These include inappropriate water chemistry (NH 3, NO 2, NO 3, ph, Dissolved Oxygen, CO 2 ) and temperature, handling, physical damage, disease treatments and incomplete nutrition. It is impossible to avoid many of the procedures known to induce stress responses in fish. Netting, grading and transport are integral components of the fish farming routine and, fish farmer should minimize the effects of this type of stress (Pickering, 1993). In general, the duration of the stress response is proportional to the duration of the stress. Thus, reducing the time-course of the event (netting, grading, transport, etc.) will encourage a more rapid recovery of the fish. A review of environmental conditions and factors that may affect welfare of common carp is given in the following sections. It is important however to realise that the environmental conditions are always defined by a range of interrelated factors and while each specific variable is described separately, there are very few occasions where only a single factor is involved in any welfare issue relating to environmental conditions. For this reason, only ranges of acceptable levels for the various factors can be given and always these should be considered in the context of the other variables involved. The EFSA Journal (2008) Annex I, 17-81

46 5.1. Abiotic factors Light period and intensity Carp, like all cyprinid fish, react to changes in light (Kezuka et al., 1988). Thus change in photoperiod regime may affect carp growth rate (Hisar et al., 2005), maturation and spawning alacrity (Peter, 1981) and respiration (Chakraborty et al., 1992). Unlike the situation in the salmonids, however, artificial change of photoperiod is not applied during the carp production cycle (Guziur, 2003). During the main part of the production cycle, when the carp are held in extensive earth ponds, fish are exposed to a natural photoperiod, which is associated with other environmental features, such as temperature. During the incubation of eggs, expert opinion suggests that light levels should be kept low to avoid stimulation of the embryo. Similarly, practical experience suggests that light levels should be kept low to avoid stimulating the larvae and disturbing them from their positions on the substrate. Over-stimulation leads to inefficient utilisation of endogenous reserves resulting in reduced somatic tissue growth. The resulting smaller larvae may also have lower survival or growth rates. There are no welfare issues of nursing fry associated with light intensity in nursing ponds because fish are not exposed to artificial light. Under normal conditions fish usually select areas with lower light intensity and are protected from exposure to direct sunlight by algal blooms and suspended solids. A sudden change in light intensity and spectrum as experienced during harvesting, grading and transport operations is a negative stimulus inducing or contributing to stress induced by lack of water, anoxia and change of position. The same considerations would apply for market fish and overwintering carp, light intensity and photoperiod correspond to ambient conditions. Light period and intensity plays role during the ripening and reproduction of spawners. However, hypophysation (see section ) is the traditional method of inducing fish to spawn (Weil et al., 1986). After moving spawners into the hatchery, especially during the hypophysation treatment carp prefer shaded places in tanks Noise and vibration There is evidence (principally from goldfish studies) that cyprinids are sensitive to noise and vibration (Smith et al., 2004 a and b; Kojima et al., 2005; Papoustoglou et al., 2007). Carp have a complex auditory system. The evidence for any significant patho-physiological effect including rupture of the physoclistous swim bladder, which cannot adjust rapidly to sudden compression, is more limited in the literature although there are reports of traumatic effects in carp subjected to major vibrations associated with seismic geological investigations (Roberts, pers. com.) Water flow Common carp do not require flowing water. Their natural habitat is slow flowing or standing waters (Brylinska, 2000). In farming conditions carp are produced in ponds without water flow, except for replacement of water losses due to seepage or evaporation. Water flow is however essential during the period of harvesting whether for market or simply to move fish to another pond, as otherwise the suspended solids generated by the close confinement and disturbance of the benthos leads to choking and suffocation of the concentrated fish. The EFSA Journal (2008) Annex I, 18-81

47 Prior to the eyed stage the developing embryo is very sensitive to physical shocks. This stage is usually reached after 24 hours at 20 C. Flow rates inside the incubation vessel during egg incubation should not exceed 1.5 litres per minute during the first hours of development and 3 litres per min thereafter (Marcel, 1990). However, Horvath and Lukowicz (1982) recommend between 0.5 and 2.0 litres/min. Water flows in excess of these rates may cause shock and possible subsequent embryonic disruption. Expert opinion indicates that, during the yolk sac absorption period, it is important that the larvae are not disturbed by turbulent waters or excessive water flows as this may result in adverse consequences such as congregation in parts of the incubation bottle and suffocation or forcing the fish to use limited endogenous energy reserves for swimming rather than somatic growth. Cessation of water flow also has the effect of concentrating the hatching enzyme released by the larvae at this stage. This enzyme weakens the chorion, making it easier for the larvae to escape, usually tail first. Excessive water flows may cause crowding of larvae and wasted use of energy reserves leading to starvation. Cessation of water flow helps hatching. Carp fry have limited swimming ability and even gentle flows can displace the fry from their habitat choice. Fry ponds are static when filled and thus there are no water flow welfare implications. Fingerling ponds are filled before stocking and thereafter no or little water flow does not have a welfare implication. Under production pond conditions, carp do not require the presence of flowing water to thrive and survive. No or little water velocity is not a welfare issue at this life stage. For market fish, water flow should provide sufficient oxygen for respiration, but should not force fish to swim against the current. If inflows are properly constructed above the water surface, they will also prevent ice forming on the surface of the pond causing interference with oxygen and carbon dioxide exchange. During overwintering, the water inflow should avoid disturbing resting fish as any increase in physical activity causes disproportionate loss of condition before the commencement of feeding in the spring. For broodstock, water quality and/or flow plays important role especially during winter, when the wintering ponds require a water flow throughout the entire winter. Adequate water supply is necessary to maintain the wintering spawners. The water flow should not be too strong to avoid mixing up the warm and cold water layers Water oxygen content Carp are remarkably tolerant to low oxygen levels, except in the first few months of the life cycle when fry are more sensitive. The amount of dissolved oxygen in the water increases as atmospheric pressure rises, but decreases when the temperature rises. These physical effects have very practical consequences. When water temperature increases, fish metabolic rate also increases but at the same time oxygen availability becomes limited. In production ponds available oxygen is also consumed by micro-organisms that decompose organic matter in bottom sediments, which also limits the availability of oxygen for fish. Occasionally, severe oxygen depletion The EFSA Journal (2008) Annex I, 19-81

48 associated with collapse of algal blooms in late summer at high temperatures can affect welfare. Because of high HbO 2 affinity, carp are tolerant to low water oxygen concentration as low as 0.9 mg/l (Albers et al., 1983) as an evolutionary adaptation to environmental conditions that occur in their natural habitat. At oxygen concentrations below ~2-3 mg O 2 /l (~20-30% saturation) carp feeding activity and hence growth rate decrease. Such low oxygen concentrations occur frequently, usually in late summer under current production technology, for the first few months of the life cycle, fry are sensitive to low oxygen concentrations. Dissolved oxygen at concentrations above 3-4 mg O 2 /l does not affect carp performance. The most frequent production technique for common carp (earth ponds, at less than kg/ha) usually provides adequate oxygen at normal stocking levels without recourse to aeration Accidental oxygen depletion, occurring in August/September, can affect fish health or cause mortality by direct asphyxia or lowering resistance to secondary bacterial infections. Such low oxygen levels usually only last for a few days. The oxygen demand of the eggs changes during the incubation period and whereas initially the demand is low, as the embryo develops, more oxygen is required (Horvath et al., 1992). Dissolved oxygen levels in the incubation water should be maintained above 6mg/l and preferably 8mg/l. At the optimum incubation temperature this equates to approximately 95% saturation. According to Marcel (1990), the levels of dissolved oxygen are very important for the hatching success as it is directly correlated to the O 2 content of water (close to 100% hatch at 9 mg/l and only 4% at 1.2 mg/l). The oxygen content also influences the hatching time which decreases with increased O 2 content (120 hours at 1.2 mg/l and 68 hours at 12mg/l). The author recommends a minimum O 2 content of 6 mg/l in hatching waters. A technique is used to synchronise the hatching of larvae. The water supply to the jar is reduced or stopped for 5 to 10 minutes producing an O 2 deficit in the water. The embryo becomes more active in an attempt to stir the peri-vitelline fluid and increase the O 2 content inside the egg. This hyper-activity synchronises the mass hatching of the larvae although careful monitoring of the oxygen levels is required to avoid any detrimental consequence of the manoeuvre. Cyprinids fry thrive when the dissolved oxygen content is between 6 and 8 mg/l. The minimum O 2 requirements for most cyprinids are low compared with salmonids. Cyprinids show signs of suffocation only when levels drop below 2 mg/l (Svobodova et al., 1993). However, fry are more sensitive to low dissolved oxygen conditions than their larger brethren. Fry are sensitive to both low and high O 2 levels. Too much dissolved oxygen in the water can cause damage to the gills: the gills appear pale, the tips of the lamellae split and secondary mycosis may result (Svobodova et al., 1993). For nursing fry, in a well-prepared nursing pond, oxygen content of water is within acceptable limits because of the balanced phyto- and zoo-plankton populations. There is a relatively low biomass of fish relative to the pond volume and there is no welfare issues associated with oxygen content. Due to the high productivity of fingerling ponds oxygen level can be a limiting factor and pond aeration is necessary, especially in polyculture ponds where up to kg/ha of fish may be harvested. In extensive pond culture, levels of dissolved oxygen rarely fall or rise beyond the optimal requirements for carp. Short term hyperoxic and hypoxic conditions can occur during the production season with possible consecutive reduction or cessation of feeding activity. Carp The EFSA Journal (2008) Annex I, 20-81

49 are however able to survive for at least a few days in water of <1 mg O 2 /l without noticeable health setback. There appear to be no welfare issues with regard to hyperoxia in case of ongrowers. During harvesting, although the normal respiration rate is low due to the cool ambient water temperature, oxygen consumption and respiration rate can significantly increase due to the stress of crowding and the presence of other bio-stressors such as poor water quality. At the same time gill efficiency is reduced due to a high concentration of suspended solids (gill clogging). Grading operations where fish are handled in little or no water can also lead to hypoxia and severe stress response (Van Raaij et al., 1996). Stress caused by handling and transportation increases the respiration rate of the fish and hence its oxygen consumption. During on farm transport, although the fish are only present in tanks for a relatively short period, oxygen levels in the water may nevertheless drop to stressful levels. Therefore additional oxygenation or aeration may be required during such transportation operations. At normal winter storage temperatures, oxygen levels will be unlikely to affect welfare. Oxygen saturation of the water inflow should not drop below 60% (6-7 mg/l O 2 ) to maintain in-pond saturation above the required levels. Ponds for breeders should be deep, and supplied with adequate water each week to prevent unwanted changes in water quality. During hatchery operations when the adults are held in tanks, oxygen requirements for the broodstock fish are around 100 mg of O 2 /kg live weight/hour in water that is saturated with oxygen. Minimum levels of oxygen are 6 mg/l (Billard, 1999) Total dissolved gases Expert opinion indicates that above a 102% level of total dissolved gases, problems can occur with gas bubble formation leading to a loss of eggs from the incubation vessel and longer term effects on surviving individuals. For larvae, the embolism manifests itself in small bubbles causing disruption of swimming activity. Damage may also occur to the yolk sac evidenced by white patches within the yolk. Supersaturation with dissolved gas occurs when the pressure of gas dissolved in the water exceeds that of the atmospheric pressure. Levels of nitrogen (as N 2 ) are toxic above 100% saturation Billard (1999). Signs of supersaturation are gas bubbles on the exterior of submerged objects and foam or bubble-scum and distressed fish on the water surface. Close examination of the affected fish usually indicates over-inflation of the swim bladder, gas bubbles in the gut and vascular system and the presence of embolisms in the gills, skin and fins. Causes of supersaturation are various and range from suction leaks on pumped water systems to intensive photosynthesis of phytoplankton and macrophytes. Vigorous aeration usually cures the problem by allowing increased contact of the super-saturated water with the atmosphere. Carbon dioxide (CO 2 ), a product of intracellular respiration, is a toxic and aversive gas. In the crowded conditions experienced in a transport tank, stripping of CO 2 from the water occurs only to a limited extent. The CO 2 concentration increases with time; even when the water is oxygenated or aerated. Prolonged transport can lead to a significant fall in the ph of The EFSA Journal (2008) Annex I, 21-81

50 the water, inhibit the ability of the fish to excrete CO 2 and cause a drop in plasma ph. Dissolved gases can raise a number of welfare issues and CO 2 is a particular concern; not only is it particularly stressful to fish but also it can affect other physiological factors such as blood ph and muscle lactic acid accumulation. CO 2 concentration at normal winter storage temperatures may rise if water surface is covered with ice. This is however of little welfare concern given the torpid physiological state of fish. During the over-wintering period, accumulation of toxic gases (e.g. CO 2, H 2 S, NH 3, and CH 4; Avnimelech et al., 1986; Ritvo et al., 2004) resulting from decomposition of organic matter can have a lethal effect on the over-wintering carp. For this reason, it is essential to maintain openings in the ice cover in order to enable continuous gas exchange Water temperature Carp are ectotherms; therefore, any significant change of ambient water temperature has an effect on most vital body systems (cellular respiration, sensory system, immune system) rate. During its domestication the common carp has adapted to European climate conditions. Production ponds provide temperature conditions almost identical to natural. The annual temperature cycle determines the temperature in ponds and thus carp activity. Carp are able to survive across a wide temperature range (from ~2 C to > 36 C), although activity changes drastically with temperature. According to Meuwis and Heuts (1957), lethal temperature for small individuals is slightly higher than for adults (respectively ~38 C for small fish and ~36 C for adults). Such high temperatures are very unusual in normal production conditions in Europe. Optimum feeding efficiency and growth rate is generally obtained between 23 and 29 C (Brylińska, 1991). Decreases in water temperature below 20 C and increases above 30 C both lead to a decline in feeding. Carp will increase weight when feeding at temperatures above ~14C (Szumiec, 1984). This means that in most European carp producing countries, there is a growth period of about days during the year (Szumiec and Szumiec, 1985). During the incubation of eggs, it is important that the temperature of the water be maintained as constant as possible within the optimal range. Short-term changes of up to 1 hour within the range 8 C to 28 C have been shown not to affect carp eggs (Jaoul and Roubaud, 1982), but efforts should be made to reduce the thermal fluctuation as much as possible. Thermal control is much easier to achieve in the hatchery situation but more difficult in natural ponds as the water temperature fluctuates in response to changes in ambient conditions. Optimum incubation temperatures for carp eggs range between 22 and 24 C. At these temperatures hatching takes place after 60 to 70 degree days (Billard, 1999). Carp larvae are very susceptible to temperature fluctuations. During this stage or during transfer from the egg incubation system to the hatching system the temperature difference should not exceed 1 C (Billard, 1995). Temperatures high in excess would lead to increase rates of body deformities. In shallow early-rearing ponds the temperatures can fluctuate by more than 22 C over 24 hours. Ponds of cm depth generally fluctuate in temperature by approximately 1 C per hour. An increase in pond water depth of only 10cms reduced the diurnal temperature fluctuation by 5 C (Szumiec, 2004). Rapid temperature change (close to 3 degrees per hour) rather than absolute limits is normally a significant welfare issue for carp fry. For carp fry, the lethal limit for temperature change as reported by Smisek (1977) and Lirski & Opuszynski (1988) is 3 C per hour. Generally, ponds with greater volumes and depths show smaller temperature fluctuations. The optimum temperature range for growth and development of carp fry is between 20 C and The EFSA Journal (2008) Annex I, 22-81

51 30 C. Special attention should be paid to temperature differences during transport of fry from the hatchery to the nursing pond. Sudden temperature changes have a detrimental effect on the fry. If temperature differences exceed 1 or 2 C, transport tanks should be placed in the pond for minutes or pond water added to the tanks to gradually equalise the temperatures (Horvath et al., 1984). During the nursing period fry will spend most time in shallow warmed waters. If there are large temperature changes fry will move to deeper parts of the pond. Thus, there are unlikely to be welfare issues with temperature in stocked ponds. As the volume of water in the pond reduces during harvesting operations, the temperature of the water is more easily influenced by ambient conditions. Direct, strong sunlight and changes (up and down) in the ambient air temperature rapidly affect the temperature of the water (Berka, 1986). A rise in the pond water temperature is highly undesirable as this increases the rate of fish respiration and microbial oxidation of organic matter originating from bottom sediment. Thus, harvest is usually done early in the morning. During grading operations, fish are exposed to temperature shocks when moved from/to water tanks and grading tables or scales. Such temperature shocks induce stress response (Tanck et al., 2000). The authors also state that subsequent chocks lead to habituation. Wherever possible, efforts should be made to equalise the water temperatures in the harvested pond, grading tanks, transport tanks and the final destination pond/tank. In most cases, the water temperature in storage ponds (marketable fish) poses no welfare problems. Water temperatures where carp are reared through the winter may range between 1 and 4 C. This will be unlikely to affect welfare. However, in abnormally warm winter conditions, the increase in water temperature may significantly increase mortality rates. Water temperature plays an important role during the ripening of spawners. Approximately 2000 degree days are required between spawnings to complete sexual maturation of the ovaries (Horvath, 1986). It is also important to ensure that temperatures do not exceed 20 C during the early part of the season as this may interfere with the ripening of the ovaries leading to resorption of the mature oocytes. The time of ovulation is dependent upon the water temperature and the number of hypophyseal treatments. When one treatment is used ovulation would take place after hour-temperature degrees. This corresponds to hrs in water of C. When two treatments are used, ovulation may be expected hour-degree (12-13 hrs) after the second treatment Water ph Adult carp can survive in waters with a wide range of ph , although extreme values reduce feeding activity and thus growth rates. Optimum ph values are between 7 and 8. In production ponds ph rarely drops to below 6, though it may often exceed ph 9 (reaching ph values of up to 11) during spring algal blooms. The effect is greater in fry ponds with low water turbidity. The direct effect of ph is less important than the indirect effect of increased ph values have on the un-ionized ammonia content. Water ph per se has little importance in carp husbandry, it is only important in terms of its influence on other abiotic hazards (e.g. ammonia) should they be present. Oyen, Camps and Wendelaar Bonga (1991) stated that carp larvae appear to be more sensitive to acid stress than other species of fish, specifically salmonids. Water acidification below ph 5.2 appeared to be lethal to the larvae. These authors determined that the critical The EFSA Journal (2008) Annex I, 23-81

52 ph level for carp eggs ranged between 4.75 and 5.5. At these levels the egg mortality was the highest and embryonic development and hatching were delayed. At ph 4.5, 100% of the eggs disrupted before hatch and in the range there was a strong increase in the spinal chord deformation. At ph 5.5 a delayed rate of embryonic development, increased mortality, delayed hatching time, elongation of the hatching period and an increase in deformities was observed. No differences were observed in the range 5.9 to 7.5. Jezierska and Bartnicka (1995) observed that both high and low ph caused inhibition and deformation during cleavage and blastula formation as well as extension of the total development time. The optimum range for egg incubation of carp was determined at between ph 6.0 and 8.5. Korwin-Kossakowski (1988) also reported similar findings indicating that the threshold below which larval development is stopped is Deformities and high mortalities occurred in this range due to the inability of the carp larvae in filling its swim bladder preventing swimming and causing death by starvation. Oyen et al. (1991) also observed that the carp larvae hatched at an earlier stage of development which could lead to increased environmental stress due to incomplete development. No differences were observed in the percentage of deformities in the ph range Korwin-Kossakowski (1992) studied the effect of alkaline water on the growth and survival of larvae: as the ph increases, growth is retarded and survival rate diminished. Jezierska (1988) reported that the oxygen consumption of carp larvae decreased from 1.8 mg O 2 per hour at ph 9.5 to 0.7 mg O 2 per hour at ph At the higher ph levels, mucus secretion at the gill surface increases and interferes with the oxygen uptake of the larvae. This may account for the lower survival and growth rates. As for fry, the lethal level was determined to be below ph 5.2 (Oyen et al., 1991). Korwin- Kossakowski (1988) reported high deformities and mortalities of fry occurred at ph due to incomplete swim-bladder inflation resulting in poor swimming ability, starvation and death. For nursing fry and fingerlings, in a well-prepared nursing pond, ph will be within acceptable limits because of the balanced plankton community and there will be no welfare implications. Water ph accurately reflects the fertiliser level of the pond. At high ph values (>8-9) chemical fertilisers with a high nitrogen content can be used only if water quality is strictly controlled since the toxic effect of ammonia is enhanced by the ph level. For on-growers, transport tanks are usually filled with water of the same origin as storage/winter ponds. Thus initially, the difference of ph value can be ignored. On-farm transportation occurs early in the spring or late autumn when water ph rarely exceeds the optimal values for carp. However, extended transport and retention within the transport tank can lead to a build-up of dissolved CO 2 and the resulting change in water ph can be considered as a potential negative stimulus. Normally, the water ph is not relevant to welfare aspects for marketable fish as they have limited physical and metabolic activity during this period. Similarly, ph values range between 6.5 and 8.5 and have no welfare implications for over-wintering carp. However, high discharges of snow melt water may result in particular low ph levels. This causes severe irritation and inflammation, particularly of the gills, and may cause mortality. Due to moderate stocking densities and well-managed pond conditions, water ph does not have welfare implications during broodstock maintenance Suspended solids Feeding activity of carp causes re-suspension of bottom sediments, resulting in high concentrations of suspended solids. Carp can re-suspend more than 4-6 times their own weight of bottom soils per day (Braukellar et al., 1994). The type of suspended matter The EFSA Journal (2008) Annex I, 24-81

53 depends on original soil composition, age of pond and feeding rate. Usually more than 95% of the re-suspended material consists of mineral particles, usually fine clay particles. Carp in production ponds are exposed to suspended solids concentrations of up to approximately 200 g/l. Suspended solid concentrations caused by feeding behaviour under most common production conditions do not affect fish health status. Suspended matter is however a serious potential problem during harvesting when fish are crowded and disturbed, suspended solids concentration in the water can increase to >10 3 mg/l. In such cases severe gill obstruction occurs and there is considerable reduction in respiratory capacity, limited gas exchange across the gills and temporary anoxia. Water supplies to the egg incubation system, according to wide industrial experience, should be filtered to remove any particulate organic or inorganic material. High levels of suspended solids in the incubation systems can result in complete encapsulation of the egg with material which interferes with the efficient transfer of oxygen across the egg membrane. This can cause egg losses especially during the later stages of development when O 2 requirements are much higher. Normally, water supplies to the hatching system are filtered through a 100 micron screen to remove any particulate organic or inorganic material. This also ensures no predatory invertebrates such as cyclopoid copepods are present in the hatchery tanks. These invertebrates cause significant damage and losses in carp larvae. High levels of suspended solids in the incubation systems can result in suffocation of the larvae and make good tank hygiene harder to achieve. For swimming fry, material suspended within the water column can come from a number of sources. Dead organic matter, colloids, fine silt and suspended minerals all contribute to the turbidity of the water. Suspended solids cause damage to the fine gill structure by the mechanical action of the particles. The harmful effect will depend on the species of carp and their resistance, on the nature of the suspended particle and its hardness or angularity (Alabaster and Lloyd, 1980). Gill damage increases significantly if the level of suspended solids exceeds 40 mg/l. However, larvae are more sensitive to suspended solids and levels should not exceed 30 mg/l (Billard, 1999). There is no known welfare issues associated with suspended solids in nursing ponds. Similarly, in well- managed fingerling ponds suspended solids will not have welfare implications. High level of suspended solids is a primary cause for water quality deterioration. During final stage of harvest, suspended solids concentrations can easily reach levels as high as mg/l (Lin et al., 2001). Carp (marketable fish) do not feed in storage ponds and therefore, if the pond bottom is adequately maintained, no re-suspension of suspended solids occurs. As long as there is no excess of silt on the pond bottom, the only source of suspended solids would be via the incoming water to the storage ponds. This is therefore not normally a welfare issue for carp in storage ponds. Suspended solids problems normally do not occur during over-wintering. Similarly, due to moderate stocking densities and well-managed pond conditions, suspended solids do not have welfare implications during broodstock maintenance Ammonia content Ammonia is the main end product of protein metabolism, often representing over 80% of the waste nitrogen. It is excreted via the gills. This product of fish metabolism and its levels The EFSA Journal (2008) Annex I, 25-81

54 within the water column are among the most important factors affecting fish welfare. The toxicity caused by this chemical is related to the level of unionized ammonia (NH 3 ) and this varies depending on the ph of the water and also temperature, with lower temperatures resulting in lower levels of unionised ammonia (Westers, 2001). Unionized ammonia levels increase with ph and levels above 0.2 mg/l can cause mortality. The precise toxic level is dependent on the life stage, with larvae and small fish being particularly vulnerable. Unionized ammonia primarily affects the gills and results in increased mucus production, followed by oedema of the secondary lamellae, hyperplasia and necrosis of the gill epithelium. Under normal carp culture conditions, total ammonia nitrogen levels rarely exceed 1-2 mg/l so welfare issues rarely arise (Kolasa-Jaminska, 2002). However, when fish are growing fast and there is intensive photosynthesis by blooming algae, and the levels of ammonia coupled with a rise of ph can cause problems. Unionized ammonia can be a serious welfare issue under conditions of intensive photosynthesis such as following collapse of algal blooms. Great care and understanding is required in levels of fertilisation of ponds to avoid this hazard. Seine netting operations have the effect of re-suspending the bottom sediments and releasing the accumulated nutrients back into the water. Total ammonium nitrogen concentration in the water can reach dangerous levels and exceed 10 mg/l (Kolasa-Jaminska, 2002; Kolasa- Jaminska et al., 2003). Un-ionised ammonia (NH 3 ) can reach potentially lethal levels, especially if the ph is high. Under alkali conditions with ph in excess of 9, a high proportion of total ammonium nitrogen exists as NH 3. Ammonia present in rearing ponds comes from a variety of sources including excretion from the gills of fish and the bacterial decomposition of organic matter or uneaten feed. The toxic effect of elevated levels of ammonia in the water is attributed to the blocking of the outward flux of ammonia excretion across the gills. This causes the levels of ammonia in fish plasma to increase (Israeli-Weinstein and Kimmel, 1998). Typical rates of ammonia excretion from common carp are between 2 and mg of ammonia per kg of fish per hour (Wood, 1993). Critical levels of ammonia will depend on other factors, but ph is a very important. Recommended maximum levels of NH 3 in pond water are 0.1 to 0.2 mg/l at ph 7 (Pillay, 1990; Billard, 1999; Horvath et al., 1992). Exposure to high concentrations of NH 3 reduces survival, inhibit growth and cause a variety of physiological malfunctions (Tomasso, 1994). Numerous studies have demonstrated that carp exposed to long-term sub-lethal levels of NH 3 suffer damage to the immune and haematopoietic systems (Wlaslow et al., 1990), blood chemistry changes (Palackova et al., 1990) and behavioural changes (Israeli-Weinstein and Kimmel, 1998). Hasan and McIntosh (1986) reported that the 96 hours LC50 of NH 3 for carp fry ranged between 1.74 and 1.84 mg/l and only slight changes followed longer exposures. Carp larvae mortalities rose to 10% when the concentration exceeded 1 mg/l NH 3. In a well-prepared nursing pond there are no welfare implications with ammonia levels. For fingerlings, and because of the intensive fertilisation and plankton growth in fingerling ponds, there is a high probability of high ph and consequently dangerous concentrations of unionised ammonia. These parameters are closely monitored. The EFSA Journal (2008) Annex I, 26-81

55 In transport tanks total ammonium can accumulate although, under normal conditions (ph close to 7), only a small fraction becomes unionized. During on farm short term transport at low temperature (spring or autumn harvest) NH 3 is therefore a minor issue, although in emergency situations (e.g. vehicle breakdown), such considerations may arise. For marketable fish, excess of ammonia and other respiration products are removed with water flowing through the ponds. Under normal circumstances this is not a welfare issue for carp in storage ponds. Due to moderate stocking densities and well-managed pond conditions, ammonia content or environmental pollutants do not have welfare implications during broodstock maintenance Pond size and morphology Since carp are grown in large to very large ponds or even small lakes, their conditions in many ways mirror those of their natural environment. During the process of harvesting fish and transferring them to other ponds or to market, sudden crowding and physical handling cause stress directly and also indirectly through considerable churning of sediments and concomitant suspended solids problems (see section 5.1.8). Over-wintering ponds are smaller than traditional ponds and these require being substantially deeper than the norm to avoid welfare issues during the coldest times. Depending on pond size, depth and stocking density, ponds can vary in their complexity. In many cases, medium size ponds (few to several hectares) have simple, uniform bottoms and are devoid of plants. In such cases, the only diversity of living environment is provided by differences in depth of the pond. The presence of shallow or deep zones allows the fish the possibility of selecting optimal temperature and light conditions. Provision of a drainage chamber and catch pit (either inside or external to the pond) and a controlled method of removing the water will reduce the stressors associated with harvesting. Catchpits in harvest ponds should be carefully designed to minimise the suspended solids problems. Pond size and morphology including design of the catchpit have a direct impact on duration of the crowding and final loading rate. A properly designed and maintained pond bottom is essential therefore to allow fish to swim down to the catchpit. If the bottom of the pond is too flat or if there are pits (or holes), a proportion of the harvested fish may be stranded. These fish may be exposed to suffocation, desiccation or predation. The pond bottom should slope evenly towards the outlet chamber without any low points in order to ensure full drainage. Banks should have at least 1.5 m of freeboard to provide shelter from the wind. Dubish ponds are typically 120 to 300 m 2 in surface and have an average depth of cm (Horvath et al., 1992). These small shallow ponds are used to spawn selected pairs of adults under semi-controlled conditions. The depth and volume of the pond is important as this determines the water temperature. Volumes of less than 150 m 3 allow the water to warm quickly after filling and the shallow depth ensures the emergent nature of the chosen substrate. During the swim-up stage the water depth of the pond or tank is important. The larvae are limited in their ability to swim and if the water depth is >1 m, they will be unable to fill the swim bladder with air. Failure to inflate at this stage causes the incomplete development of the swim bladder, gives rise to impaired swimming ability and results in poor health and slow growth rates. The EFSA Journal (2008) Annex I, 27-81

56 Typically, early rearing ponds for carp fry range in size from 500 to 10,000 m 2 with an average depth of m and situated in areas sheltered from the wind (Billard, 1999). Ponds of this size can be drained and refilled quickly, can be protected from predators and warm up rapidly in the spring. Larger deeper ponds would be more difficult to maintain. Storage ponds should be around 2 m deep in order to reduce the effect of changes in ambient air temperatures. Shape and slope of the bottom and the design of the catch pit should ensure rapid and efficient fish crowding. Concrete bottoms should be avoided as they may result in traumatic skin lesions (see above). When a pond is partially emptied, suitable equipment should be used to prevent physical damage to the remaining stocks as well as to the harvested fish. The ponds used for over-wintering carp, should fulfil special requirements to avoid poor welfare or mortality. They are m deep, and should have a soft bottom with a low proportion of organic matter. The pond should be supplied with some water flow to prevent ice formation. It is important that over-wintering ponds are sufficiently deep for the coldest weather. The sizes of ponds used for maintaining broodstock varies greatly. Generally, in colder regions, the broodstock are held over-winter in deep (1-2m) 1000 m 2 ponds at densities of between 100 and 450 individuals (average size 5-6 kg) (Billard, 1999). The number and size of ponds used for this purpose are proportional with the size and number of broodstock, maintained by the given farm. For the short period after wintering males and females should be kept in separate ponds. They can be mixed in one pond after completing the reproduction/propagation season Substrate of ponds The feeding activity of carp tends to remove all vegetation from the pond bottom and the constant stirring leads to the formation and deposition of a fine sediment. This is less of a problem in very large ponds. Unless ponds are managed carefully, silt can build up to a considerable depth and lower layers of this silt, if undisturbed, become anoxic. This favours the production of toxic substances. This is important in terms of the fish but also leads to off flavours in the flesh. The constant grubbing of the bottom of the pond means that there is little opportunity for growth of plant life other than reeds. This means that, since carp require plant substrate on which to deposit their sticky eggs (Mills, 1991), spawning ponds have to be carefully managed to ensure weed growth or else artificial substrates have to be introduced at appropriate times. On contact with water the eggs immediately become sticky and adhere to any available substrate. In controlled carp production, this substrate can either be natural (aquatic macrophytes), flooded terrestrial vegetation (grass, etc.) or artificial materials (polypropylene strips, woven polyamide materials, nylon brushes, etc.). Basic requirements for the choice of substrate are that it should be non-toxic to the eggs, have a large surface area, preferably be soft and flexible and have a dark coloration. On hatching the larvae also require access to substrate onto which they can attach themselves using the cranial gland. Proper preparation and cultivation of the pond bottom is essential in order to ensure a suitable habitat. Over the previous production cycle, silt will have built up rapidly as a result of algae die-off, introduction of supplementary feed and the actions of the carp themselves. During the winter, dry ponds are cleaned and hard-stemmed plants removed. Before filling, and between repeated use of the pond for new stock, the pond bottom and sides are disinfected with lime at kg per ha (Horvath et al., 1984). Exposure to the air, sun The EFSA Journal (2008) Annex I, 28-81

57 and frost are essential as this helps to oxidise and break up the deposits, some of which are anaerobic, and also to kill some of the parasites and their vectors. When desiccation cracks are evident in the mud, the deposits need to be aerated, usually by tilling or removed in the case of excessive build up. Failure to prepare the pond for the coming season can lead to problems with water quality, excessive macrophyte growth and problematic harvesting. Direct disinfection of the pond bottom is important to ensure control of parasites and their intermediate vectors. A number of materials are used, the most common being quicklime (CaO). Dosage varies but generally rates range between 300 and 1000 kg/ha. After few days, the pond should be flooded and ph controlled (<8.5) before proceeding with water exchange. The build-up of excessive amounts of soft sediment with high concentrations of organic matter in on-growing ponds should be avoided as this favours the production of toxic compounds such as H 2 S, and CH 4 (Avnimelech et al., 1986; Ritvo et al., 2004). These compounds when released into the water body can seriously affect the carp. Excess of soft sediments may cause welfare issues associated with clogging of the gills of marketable fish. Storage ponds should not have concrete bottom as it results in skin lesions to ventral surface of the body. For over-wintering carp, the substrate should not have a high organic content as this may increase oxygen consumption within the substrate and production of toxic gases (e.g. H 2 S, NH 3, CH 4 ). On the other hand, hard substrate should be avoided as this may damage the ventral body surface of the carp resting on the bottom. Broodstock ponds are usually-maintained and managed in a way that substrate of ponds does not normally have any welfare impact. During the pre-reproduction period, when breeder fish are separated by sex, ponds are free of any higher vegetation in order to avoid basic environmental conditions (submerged plants) for unintentional/unwanted natural reproduction of carp Environmental pollutants Carp ponds are relatively stable and do not normally have any substantial water inflow, but there is some replacement water for evaporation and rain can bring terrestrial pollutants into the system. The majority of the European carp farms get the water required for farming from natural water flows (mainly from rivers and canals), where organic or inorganic pollution can occur. It is not always possible to prevent pollutants from being introduced to ponds, especially with barrage-type ponds. Agricultural pollutants are occasionally problematic, either as contaminants of the incoming water or via aerial spraying drift, or terrestrial run-off and there is a wide literature of specific toxic effects of specific environmental pollutants on carp. De Boeck et al. (2006) showed that copper exposure, often used as a parasiticide, reduced swimming capacity of fish Environmental conditions biotic factors Algal blooms Algal blooms may affect welfare of fish in three different ways. First, because their photosynthesis levels are so high, their metabolites can cause dramatic increases in pond ph to levels that may be toxic either directly or through increases the proportion of unionized ammonia to toxic levels. Secondly, in many cases the algae involved may include toxigenic cyanobacterial species, which can on occasion cause mass mortality. Thirdly, when the The EFSA Journal (2008) Annex I, 29-81

58 bloom collapses, the oxygen may be extracted from the water column at a very rapid rate, and this can lead to significant mortality (McNeill and Closs, 2007). Intense algal blooms occur on a regular basis in carp culture ponds. This is especially true when young fish are being reared as they crop large numbers of phytoplankton grazers such as rotifers and crustaceans. During these blooms, high levels of photosynthetic activity lead to an increase in the ph of the pond water. Levels as high as 10.2 are regularly recorded and this leads to problems with ammonia toxicity, dissolved oxygen levels and gas supersaturation. At ph 7 and temperature 24 C, only 0.5% of the total ammonia is present as NH 3. When the ph rises to 10.2 at the same temperature, 89.3% of the total ammonia is present as NH 3. Saturation of O 2 due to high levels of photosynthesis during warm sunny periods regularly reaches 250%. At these levels, bubbles of oxygen can form internally and on the skin of the fry forcing them to the surface. During prolonged periods of dull, calm weather the opposite situation will occur. Algae become net-consumers of oxygen and levels can drop to lethal limits. Without supplementary aeration, significant mortalities (up to 100%) will occur. Cyanobacteria can produce several potent toxins as secondary metabolites. Osswald et al. (2007) demonstrated that cell counts of Anabaena sp. above 10 7 cells ml -1 caused 100% mortalities after 26 and 29 hours exposure to the toxin whereas exposure to 10 5 cells ml -1 no deaths were observed Behavioural interactions The aspects of the behaviour of common carp that are relevant to their welfare include the way in which they move about their environment, their interactions with members of their own species and their interactions with members of different species. In general, the senses of common carp are the same as for other fish, but olfaction is particularly important. Cyprinids make extensive use of chemical cues when tracking resources, interacting with con-specifics and avoiding predation (Sorensen and Stacey, 2004). Common carp therefore live in a rich and complex olfactory world of which humans are largely unaware and this has implications for their welfare when they are farmed. Common carp placed in an unfamiliar area undergo a period of exploration (the length of which varies among individuals) before restricting their movements to well-defined home ranges (Crook, 2004). Home ranges can change with season, as conditions become unfavourable and fish disperse. During winter, undisturbed common carp concentrate their movement in deeper water, avoiding shallow edges of the pond. They continue to move about (between 20 and 60 m/day) within this area, even at temperature below 4 C (Bauer and Schlott, 2004). When oxygen levels fall, fish leave the deeper water and move to shallow areas near the inflow in search of water with higher oxygen levels (Bauer and Schlott, 2006). This has implications for welfare, since small, heavily-stocked over-wintering ponds may not offer the fish scope for movement and continued feeding. Various features of the interactions of common carp with members of their own species have implications for welfare under farmed conditions, including formation of social groups, competition for resources and courtship and mating. Many cyprinid species live in social groups. When the fish all swim in synchrony, these are called schools; when they move around in a less coordinated way, these are called shoals (Pitcher and Parrish, 1993). Common carp are no exception and in nature spend most of their lives swimming around in close proximity to shoal-mates. Living in a group protects fish against predators and also helps in finding food. Naïve common carp learn more quickly to associate a sound with the presence of food when in the presence of a companion that has already learned the task (Zion The EFSA Journal (2008) Annex I, 30-81

59 et al., 2007). Isolated fish are strongly motivated to join a social group (Scangos (2004) cited in Thomson and Walton, 2004). The implications of this strong shaoling tendency for welfare of farmed carp are positive, since farmed carp are unlikely to be deprived of companionship. In common carp, overt aggression over food is rare and competition mostly takes the form of a scramble. Since common carp are often produced in polyculture with other species interactions with other species include potential competition for food and, more importantly in a welfare context, predation (see section 5.2.3). In polyculture, tench and common carp show up to 60% overlap in diet, but carp still grow well (Adamek et al., 2003). Another major problem for fingerling production is the presence of harmful fish species, such as Prussian carp (Carassius auratus gibelio) and topmouth gudgeon (Pseudorasbora parva), which enter the ponds as larvae when the ponds are filled. These species are direct food competitors with carp and in the case of similar inputs will decrease the yield of carp fingerlings Predation Especially when small, fish fall prey to a wide variety of predators including mammals, birds, other fish and also invertebrates. Common carp are no exception even in culture ponds. Where prey fish co-exist with potential predators, they can protect themselves against capture by early detection of the predator, which in turn depends on maintaining an appropriate degree of vigilance. Cyprinid fish, including common carp, produce a specific alarm substance in specialised cells in the epidermis when is released when these cells are ruptured from the damaged epidermis of a fish which has been attacked (Pfeiffer, 1977). Alarm substance can elicit specific escape responses, but also prompts fish to move away from the area in which it is detected. Cyprinid fish are also able to detect the scent of predators and, from the scent of their faeces, to recognise what species of fish the predator has been eaten, and therefore how much of a risk it poses. Group living represents a particularly striking anti-predator adaptation in fish (reviewed in Krause et al., 2002). Since information transfer within schools or shoals is rapid, fish in groups detect predators sooner and so have a better chance of escape than single fish. If a predator does attack, living in a group increases an individual fish chance of escaping capture through a simple dilution effect. In addition, the various manoeuvres that schooling fish perform when attacked serve to confuse the predator, to the extent that the attacks often fail. Thus the strong schooling response of common carp is a critical part of their protection against predators. The existence of this suite of anti-predator responses in carp has implications for their welfare when farmed. Farmed carp may be attacked by piscivores such as birds and aquatic mammals (Adamek et al., 2003 and 2007). They may also respond to indirect signs of danger, such as alarm substance if any fish are damaged. Perception of apparent predation risk may reduce feeding in farmed fish through trade-offs between protection and feeding. Carp husbandry systems in Europe allow normal social interactions. Predation is a serious welfare issue particularly significant in the farm pond environment where cormorants in particular can induce significant stresses manifested by behavioural modifications and associated reduction in feeding. Great cormorant, Eurasian otter and grey heron are among the most significant fish predators damaging carp production. On-growing carp are especially vulnerable to the predation due to their easy availability due to their optimal size and high stocking densities. The damage caused by cormorant predation pressure does not consist only of losses due to their direct predation. There are considerable subsequent indirect losses elicited by cormorant feeding The EFSA Journal (2008) Annex I, 31-81

60 activities. These result not only in fish wounding with possible secondary infection but also severe stress across the whole population of fish in the pond. The lesions on stricken fish, which have escaped from cormorant attack or which cannot be swallowed due to their size, are often deep or may be extensive surface injuries, which are a frequent precursor to subsequent infection and mortality. Hunting cormorant flocks may drive the pond fish stock into littoral zone, where the stressed fish may remain for some considerable time after the initial cormorant strike. Cormorant strikes are among the most significant welfare issues affecting on-growing carp, which is a considerable proportion of the carp life span. The majority of problems associated with otter predation on fish ponds arise in winter months, especially during the period when ponds are ice covered. Serious damage to over-wintering fish stock do not occur just as a result of direct consumption but are also due to fish being disturbed by hunting otters (indirect losses), which can lead to weight loss and increasing susceptibility to infection and parasite infestation Stocking density Stocking levels in carp pond vary depending on the farming system, the nature of the pond, whether it is winter or summer and whether there is to be auxiliary feeding (see also 5.4.1). The most common practice in pond farming under conditions of temperate climate, however, is to stock fish at a biomass of about 300 kg/ha. Because of the carp propensity for shoaling, the biomass will often be much higher in particular areas of the pond. There is no evidence that production of carp under such conditions is in any way stressful for carp. Indeed, there is evidence that any significance decrease of stocking density may exert a negative effect on growth rate and increased mortality (Wolny, 1962; Stegman, 1965 a, b). Horvath and Lukowicz (1982) indicate that between 1.0 and 2.5 litres of eggs should be incubated in 7 litre Zuger jars. Horvath, Tamas and Seagrave (1992) advise 1.0 to 1.5 litres of swollen eggs per 7 9 litre jar as the optimum loading rate. Billard (1995) recommends 1.5 to 2 litres of hydrated eggs per 7 litre jar. Higher loading rates than those indicated can lead to losses due to insufficient dissolved oxygen. Recommended figures for holding densities of newly-hatched carp larvae vary considerably. Horvath, Tamas and Seagrave (1992) and Billard (1995) suggest up to 500,000 can be held in a 200 litre container during the yolk absorption stage. Kouril and Hamackova (1991) recommend up to 100,000 larvae in 1000 litre tanks. Larvae holding densities should be appropriate for the substrate and oxygen availability. Maintaining larvae at high densities make removal of mortalities, egg shells and general tank cleaning much harder. Carp production in Central and Eastern Europe is commonly practised at extensive densities. This limits the biomass of carp in the ponds to approximately 1,500 kg/ha (depending on pond fertility) and assumes that the majority of food consumed is produced naturally within the pond. At these production densities, loading rate is not a welfare issue. However, during harvesting (see glossary) operations the biomass load gradually increases as water volume decreases. The fish become crowded, physically encounter each other and find it increasingly difficult to express normal swimming behaviour. The potential for injuries caused by other fish such as skin lesions, scale loss, split fins and broken fin rays also increases along with the possibility of transferring pathogens (mainly parasites). During the crowding period bio-stressors increase and high plasma cortisol levels are found in the fish (Huntingford, Pilarczyk, & Kadri, submitted). The EFSA Journal (2008) Annex I, 32-81

61 During transport operations, loading rate is closely related to water quality. Recommendation of fish biomass in transport tanks taking into consideration water quality has been presented by Berka (1986). Apart from the biomass welfare issues already explained above, within the transport tank injuries from the pressure of fish and contact with items such as aeration devices and valves may also occur. Marketable fish are held in storage ponds at much higher density, compared with production ponds (up to kg/m 3 ). This limits the ability of carp to express normal swimming behaviour. However carp are normally shoaling fish and at cooler temperatures, activity and mobility are anyway significantly limited. Biomass load depends on the availability of a suitable water supply to the storage pond. Depending upon the age of the fish and the pond quality, the stocking density in overwintering ponds may range broadly Food and feeding Because carp are almost exclusively produced in semi-intensive pond farms or under extensive conditions, feeding is only practised to complement the energy and protein requirements provided by pond primary production (algae, zooplankton, macro-invertebrates, etc.). Large amounts of grain (corn, wheat, triticale, etc.) and to some extent industrial byproducts (e.g. extracted grape seed, sunflower seeds) are used especially during the summer when the feed uptake of the fish exceeds the available natural feedstuffs. There is only a limited amount of formulated (pelleted) feed used in fingerling production and for broodstock. Formulated feed is often of poor quality due to (a) the use of low quality fishmeal, (b) low-level production technology, (c) unsatisfactory control of the available raw materials and feeds, (d) insufficient or inadequate lipid content in the feed, and (e) lack of equipment to enrich the lipid content of pellets. At temperatures below 5-8 C, carp normally stop feeding and utilize their metabolic reserves. They may lose up to 10% of their body biomass during such periods without any harmful consequences. The ability to withstand periods of food scarcity depends primarily upon water temperature. When deprived of food at water temperatures that are high, even though within the carp optimal temperature range, they will exhaust their fat reserves and during long periods of starvation start to deplete muscle proteins. Fish may lose a considerable proportion of their biomass (up to 30%). Long term periods of food scarcity usually occur during winter in temperate climates. Artificial feeding is used to supplement natural feed where there is a shortfall. Larvae and early fry stages require the pond to be pre-prepared to ensure adequate levels of correct feeding material or else they may be provided with artificial feed until such times as more natural feed is available. The quality and quantity of feed should correspond to the stocking density, the actual standing crop of fish and the manuring/fertiliser system. Proper preparation and management of the pond is essential to ensure a supply of natural food for the fry (see also 5.4.1). During the winter, dry ponds are cleaned and hard-stemmed plants removed. Before filling, and between repeated usage of the pond for new stock, the pond bottom and sides are disinfected with lime (Horvath et al., 1984). Tilling of the pond bottom aerates the soil and improves plankton production. Fertiliser is mostly added to the water to promote the growth of plankton. Nursing ponds are half filled 5-7 days before stocking and completely filled when fry are stocked. Nitrogen fertilisers are mixed in pond water at kg per ha. Half of the total amount is added when the pond is filled and the remainder in two applications after the first and second weeks of nursing. Phosphorous The EFSA Journal (2008) Annex I, 33-81

62 fertilisers are added when the ponds are filled. The dose rate is 100 kg per ha and the fertiliser should be dispersed over the greatest possible pond area (Horvath et al., 1984). The natural food has a synergistic effect on utilization of artificial feeds (Ruttkay, 1987). Unbalanced diets may result in loss of valuable protein due to the conversion of the protein to energy (if the food rich in energy is not applied in sufficient quantity) or to accumulation of fat if the fish are overfed with energy-rich fish feeds (Ruttkay, 1988). Dietary toxins may occur in carp feeds if inappropriately stored. Feeds can become contaminated by, fungi such as Aspergillus fumigatus or Aspergillus flavus. Their metabolites are toxic to carp even in very low concentrations (Svobodová et al., 1987; Olufemi et al., 1983). The metabolic product of Aspergillus flavus is an aflatoxin, which leads to aflatoxicosis resulting in liver tumours. Carp is more resistant to this aflatoxin than rainbow trout, which is vulnerable to concentrations less than tens of micrograms per kg of ingested feed (Hendricks, 2002). Inappropriate storage of feed cereals may result in Fusarium growth. Concentration of fusario-toxins, metabolytes of Fusarium, below one mg per kg of feed cereals is highly toxic to common carp. Carp may be intoxicated also by alkaloids produced by ergot (Claviceps purpurea), living on cereals. Despite its quite low toxicity, its presence in feed leads to histopathological alterations (Svobodová et al., 1987). After the larvae have absorbed the majority of the yolk sac and the period of endogenous feeding has almost finished, there is a mixed feeding period when larvae begin to seek external food. During this exogenous feeding period it is vital that larvae be provided with adequate feed in terms of quantity, quality, and size. First feeding is the most important phase in the early rearing of carp. Failure to provide the correct diet will lead to welfare issues including poor growth rate, increase in deformities and the incomplete development of the gut. Damage to the larvae caused by using an inappropriate feeding regime cannot be reversed at a later stage. In terms of quantity, the larvae are fed ad lib although great care should be taken not to foul the water by using excessive feed. Regular removal of uneaten feed and any dead fish along with a thorough cleaning of the rearing tanks or troughs is vital. A number of artificial particulate starter diets are available but these generally, do not perform as well as live feeds. However, producing and feeding a live diet can be expensive both in terms of manpower and cost and specialist equipment and expertise is required. A number of types of feed can be used ranging from the simplest which is finely ground hard-boiled egg yolk to the expensive but more effective live nauplii of Artemia or Brine Shrimp. Live feeds are more desirable as they contain autolytic enzymes and are much easier for the larvae to assimilate. Cyprinids are agastric (as opposed to monogastric fish such as trout) and assimilation of diet is more difficult, especially during the early life stages as the enzymes required to break down the feeds haven t had time to fully develop. Providing feed of the correct size is also important as larvae have limited ability to capture larger feed items than the mouth gape will accommodate. When the larvae are fed for the first time the size of feed introduced into the rearing tank should be between 80 and 180 microns. This corresponds to the size of Rotifera that Carp larvae initially feed on in the wild. The larvae grow rapidly under these optimal conditions and the size and quantity of feed introduced into the tank needs to be adjusted. Khadka (1986) reported that with increasing age, larvae were able to incorporate progressively larger food items into their diet. The EFSA Journal (2008) Annex I, 34-81

63 At this stage, the gut of the larvae can easily be inspected with a low-power microscope to confirm that feed is being consumed. Under natural circumstances and in pond culture, carp larvae select motile protozoans and rotifers as the first feed. Natural food develops in the ponds in response to the management programme of bottom preparation, filling and manuring. Initially bacteria are present followed by algae, motile protozoans, rotifers and finally crustaceans. Prior to stocking out the larvae, an assessment is made of the biomass of rotifers present in the receiving pond. Horvath et al. (1992) recommend that 100 ml of pond water be filtered, and the resulting filtrate poured into a clear graduated tube. Formalin is then added to kill all the plankton and the solution left for a few hours to allow settlement. If the volume of plankton present is in the range of ml, the pond is suitable for stocking. Larval feed should contain 40-50% protein. The size of food particles is extremely important since first feeding fry can consume food of only a few hundred microns in size. In the later part of the nursing period fry may consume feed up to 1 mm in size. The quantity of artificial feed is difficult to define and depends on the abundance of zooplankton, and on the survival rate and age of the fry. Initially fry require kg food/100,000 fish. Depending on the appetite of the fry the amount may be doubled during the later period of rearing. It is essential to provide only as much feed as will meet the nutrient requirements of fry. The timing of the stocking is also important as the development of the food chain within the pond continues at a rapid rate. Delaying the stocking by just a few days past the optimum rotifer window can cause problems due to the development of large numbers of predatory invertebrates such as cyclopoid copepods. Piasecki (2000) found that predation on carp fry by cyclopoid copepods increased as the supply of their preferred food (rotifers and ciliates) decreased. When the fry reach 7-8 mm long, they are resistant to attack from the cyclopoids and begin to actively seek them as a feed item. For nursing fry, after correct preparation, rotifers introduced into the pond with the water will reproduce rapidly and after 5-7 days be present in large numbers ready to meet the initial feed demand of fry. A rotifer biomass of 2.5 ml per 50 l of pond water is an optimal concentration. As fry grow they will consume more food and eventually the zooplankton population in the pond will be insufficient to meet their needs. The initial rapid growth of fry may cease and if they become weakened they will be more susceptible to disease. This may be prevented by supplementary feeding. Fry do not consume artificial feed during the first 3-4 days after stocking but it is advisable to begin supplementary feeding immediately after stocking to accustom the fish to the artificial diet. The diet will also act as an additional fertiliser for the plankton population. It is most important in fingerling ponds to maintain the production of natural food, both to maintain a healthy diet for the fish and to economise on supplementary feeding. The ratio between natural feed production and supplementary feeding is 40:60 or 30:70. The application of fertiliser starts before or immediately after pond flooding. Organic fertilisers are the most effective and are applied at kg/ha. Lime and chemical fertiliser (NPK) can also be used (Horvath et al., 1984). The optimum quantity of fertiliser to be used depends on the soil and water characteristics. It is crucial that by the time the pond is stocked the pond water should have a rich plankton fauna to support the fry. The EFSA Journal (2008) Annex I, 35-81

64 Fertiliser application continues throughout the growing period. This is especially important in polyculture where fish utilise much more feed than in monoculture. The quality of zooplankton should be 2 ml per 50 l pond water in the first half of the growing season and 1 ml per 50 l in the second half (Horvath et al., 1984). Ponds populated mostly or only with herbivorous species require 20-40% less fertilisers than common carp in monoculture since the herbivorous fish feed on water plants and recycle nutrients back into the pond after digestion. Fry require good quality supplementary feed with a digestible crude protein content of 25-30%. Mixtures of cereals or legumes, or industrial by-products are used. If the natural feed (protein) supply runs out during the growing season a high protein diet based on fish or meat meal should be given. The particle size of supplementary feed is extremely important. Particle size should be homogenous and appropriate for ingestion by the fish otherwise pellets will not be consumed. Particle size will increase as fish grow. Supplemental feeding is started immediately after stocking with fry. Initially feed should be provided in shallow water close to the pond edge but can be provided in deeper water as fry grow. Automatic feeders may be used in ponds up to 2 ha in size. In larger ponds feed is distributed by boat. The development of the eggs is directly dependent on the quality of the diet during the initial year of growth of broodstock fish (Horvath et al., 1984). Composition of the diet should include animal protein. In order tp provide the necessary amino acids for optimal growth. When holding ripe spawners (both males and females) the development of sexual products, especially eggs puts considerable strain upon the organism. To produce eggs and sperm optimal environmental and nutritional conditions have to be guaranteed for the spawners. If the fish farmer does not feed the spawners, parallel with the increase in water temperature in the spring, the fish will lose weight and become more susceptible to various diseases. When the water temperature rises above 6 C, supplementary feeding with protein rich (30-40%) pellets containing the essential fatty acids commences. In the spring, diets rich in carbohydrates and saturated lipds are avoided as these produce fat accumulations in the fish (Billard, 1999). These lipid bodies can, in extreme cases, interfere with oocyte maturation and impair spawning performance. In the larger storage ponds more natural nutrients will develop and will form pond organisms and will serve as optimal feed for the fish which start feeding early in the spring. The summer diet used after spawning should provide energy feeds for yolk production in the eggs which accumulate in the ovaries during the summer period Husbandry and management Stocking Stocking in outdoor ponds is a stressful experience for fish at all stages of development, but the early life stages are particularly sensitive and susceptible to environmental change. Transport to the pond should be done as quickly as possible and with the minimum of handling. Great care should be taken to ensure that the fish are not subjected to a rapid change in water temperature, ph, dissolved oxygen or water quality. Acclimation can be achieved by introducing the fish gradually to the environmental conditions present in the receiving tank or pond. During the early rearing phase, correct timing of stocking into the pond is vital if pond culture techniques are used. The plankton community in the receiving pond should be monitored to ensure optimal conditions for the larvae. Failure to ensure that ponds contain The EFSA Journal (2008) Annex I, 36-81

65 the correct type, size and amount of natural food can cause starvation leading to deformities, poor growth rates and high mortality. The number of first-feeding fry varies according to the abundance of natural food in the receiving pond. Billard (1999) recommends filtering 100 ml of pond water through plankton net (60-80 microns) to determine the stocking density. If the filtered quantity of plankton obtained is 1-3 ml, the pond can be stocked with between 400 and 600 larvae per m 3. Horvath et al. (1992) recommend fry stocking densities of between 100 and 600 fry/m 2 and Marcel (1990) suggested that fry/m 2 be stocked if 3ml of rotifers were present after filtering 100 ml of water. Stocking fry into ponds with insufficient supplies of suitable food will result in low survival rates, poor growth and significant deformities. Food supply is the main factor governing appropriate stocking density. For nursing fry, stocking density is always dependent on the productivity of the pond and thus the abundance of feed organisms. Generally 1-2 million fry are stocked per ha. With proper chemical treatment for rotifer propagation, fry density may be raised to 5-6 million per ha. At stocking fry should be distributed along the wind-protected shoreline of the pond. In polyculture common carp usually forms the majority of fry stocked. Other species are stocked at a much lower rate. Grass carp are stocked at the lowest level. Fingerling production of common carp and the other carp species may take place in separate ponds. Stocking rates will vary according to pond productivity and feeding strategy K of fingerlings (all species) can be produced in 3-5 ha high productivity ponds or in 7-10 ha if productivity is only moderate. Average body weight of fingerlings at harvest will be g (Horvath et al. 1984). During broodstock maintenance optimal conditions are required. In respect to stocking density this would mean an under-stocking compared with the on-growers. Depending on the quality of the pond spawners may be stocked in one hectare. After the reproduction season, recovered and healthy fish should be stocked into ponds where they can be kept until the late autumn harvest or even until an early spring harvest. When feeding these spawned-out fish, which are separated into a post-spawning pond, adequate feed should be allowed. The spawned fish will lose 10-20% of their body weight in sexual products. For the reproduction of new eggs an energy-rich feed is required to promote renewed yolk formation. The main purpose and vital function of brood stock is reproduction of sexual products, therefore a significant increase in body weight is not expected if sufficient eggs and sperm are produced. Spawners are selected and the best specimens stocked into wintering ponds at the time of autumn fishing harvest. Several hundred spawners can be kept over the winter in a wintering pond of m2 if appropriate water supply is available. During the on-growing phase, fish are held at densities greater than would be experienced in the wild and they compete with each other for resources. In intensive systems, where significant amounts of supplementary feed are used, it is important that the feed used is appropriate in terms of size, amount and nutritional profile. During low temperatures of winter, carp do not feed and are normally maintained in smaller and deeper ponds provided with an inflow of good quality water (Horvath et al, 1984). Pond substrate should be soft but free of excessive mud. The EFSA Journal (2008) Annex I, 37-81

66 Handling and harvesting Newly-hatched larvae are extremely fragile and should never be removed from water. They should be handled with extreme care to avoid physical damage. When transferring them between systems they should either be siphoned or bailed using bowls. At no time should they be netted and taken out of water. After 3-4 weeks in the nursery pond fry are mm in length and g in weight. They should then be harvested and transferred to rearing ponds (Horvath et al., 1984). Harvesting and transportation should be carried out with the greatest of care. Feeding is stopped one day before harvest. The pond is then partially drained through a fine net taking care that the flow of water does not press the fry into the net. In larger ponds, as draining proceeds, the fry accumulate in a few hundred m 3 in front of the drain from which they may be fished with fine seine net. Any remaining fry may be captured from capture boxes or drainage nets after the pond has been completely drained. Nursed fry are normally stored for a few hours before transport (Horvath et al., 1984). They are usually held in 5-10 m 3 fine mesh rectangular nets held near a pond outflow. Such nets may hold 200, ,000 fry for a few hours. Fry are less susceptible to damage if transferred directly to the transport vehicle. Nursed fry are counted volumetrically in water before transfer to the transport container (Horvath et al., 1984). During transportation adequate oxygen should be supplied. Nursed fry at 70, ,000 per m 3 of water may be transported safely for several hours. At high temperatures transport water should be cooled by placing plastic bags of ice into the transport tanks. In the context of carp farming, harvest means the de-stocking for the purpose of transfer of fish to another pond or facility or to market. Harvesting of ponds is a critical operation in respect of handling fish. It is particularly problematical in polyculture where production may be very high and harvesting is hindered by a restricted harvesting area. In larger ponds the need for netting is removed by the use of a fish bed into which the pond is drained. This allows preliminary sorting of fish as different species respond variably to the water current. Thus, herbivorous species leave the pond before common carp, tench (Tinca tinca) and Wels catfish (Silurus glanis). Fish are sorted by hand or by mechanical graders. Once graded, fish should be retained in storage areas for a period before transportation, especially if the latter takes more than 30 minutes. This is particularly important for silver carp. The majority of carp produced in the EU are grown using pond culture. Harvesting the ponds usually commences in October when water temperatures have dropped below 14 C. Below this temperature, carp have a significantly reduced metabolic activity and their requirement for oxygen is diminished. During harvesting operations the fish are crowded and this is one of the most stressful aspects of carp culture. Fish are removed from the pond by partial drainage and seine netting or by complete de-watering. In the case of complete drainage, the fish are concentrated within the pond in a catchpit immediately in front of the outflow chamber or in a purpose-built structure external to the pond. Fish are removed manually or by using a variety of mechanical means, such as airlift and vacuum pumps, Archimedes screws, conveyors, landing nets or large buckets (Lanoiselee and Varadi, 1999). During this phase, damage can occur to the fins and the fish may suffer loss of mucus, scales and areas of skin. This leaves them open to infection from bacteria, viruses and secondary mycosis. The EFSA Journal (2008) Annex I, 38-81

67 Harvesting operations can also disturb bottom deposits, most of which are anaerobic. This can lead to low dissolved oxygen content in the water and anoxia. Efforts should be made to maintain the fish in water of sufficient oxygen content, either by removing the fish as quickly as possible or by introducing fresh, oxygen-rich water into the catchpit. High levels of some types of suspended solids can also cause significant damage to the delicate gill filaments. Harvesting of on-growers should be done as fast as possible to minimise period when carp welfare may be compromised. Timely, efficient and effective sorting, grading and weighing are crucial to avoid hypoxia and damage of harvested fish. Slow harvesting operations usually occur because of lack of planning, poor staff training, and insufficient resources (manpower and equipment). Once fish are harvested they are held in clean, running water to induce them to swim against the current to allow them to flush out their gills. As the volume of water in the pond decreases and individual fish are forced to break the water surface, this represents the onset of critical crowding. During these final stages of the harvest, fish may be crowded further, using nets of different types (seine, pole-nets). This practice is commonly carried out to increase the efficiency and effectiveness of the process. However, this further increases the opportunity for physical traumatic damage to the fish skin. Whenever possible, fish should be handled within water to ensure even hydrostatic pressure on body. Out of water, fish are exposed to unidirectional gravitational pressure which places very different pressures on circulation and organ systems. In storage ponds, marketable fish are generally handled mechanically and may be subject to various operations (netting, weighing, and transport) during the process of delivery. These operations may on occasion unintentionally cause physical lesions. This would be a welfare issue although generally, since fish are marketed on quality, care is taken not to create such lesions. During the over-wintering period, considerable care should be taken not to disturb the carp. However, during the periods of transfer into wintering ponds and their subsequent transfer out there are handling events with which significant welfare issues may be associated. These are very similar to those described in relevant section for on-growers and the necessary precautions are the same Handling of broodstock Separation of Sexes Spawners need to be separated by sex when water temperatures reach 8-12 C (March-April). This is necessary because mixed stocks are inclined to spawn naturally and thereby sexual products will be lost for the induced and programmed propagation. At this stage of development, enamel white milt will appear in the males with even a slight pressure, while females will have medium soft bellies swollen because of the developing ovaries. After separation of the sexes, feeding should be increased (Horvath et al., 1984). Propagation in a strict sense starts when spawners, previously separated by sex, are moved into the hatchery (Horvath et al., 1984). Fish already sorted several times should be examined and the ripe developed specimens selected. Less developed spawners will be selected later since even in fraternal stocks there may be considerable differences in the development of individual fish. The EFSA Journal (2008) Annex I, 39-81

68 Large scale propagation of common carp is economical when the number of female spawners available is appropriate for the facilities of the production farm (e.g. number of ponds to be stocked at the same time). The number of female spawners is the limiting factor as the propagation process will not be restricted during the short spawning season by a lack of males or hatching facilities (Horvath et al., 1984). Induced ovulation of spawners is done in tanks or in special small ponds depending on the facilities available on the farm (Horvath et al., 1984). Spawning in tanks under shelter requires more sophisticated technical equipment. Several small ponds are simpler and can be suitable for mass propagation, but are less controllable and more difficult to mechanize, involve more manpower and a greater loss of eggs. For tank operations the water requirement is about 4-6 l/min for one spawner and can be reduced by aerating the tank or using oxygen. A further advantage of spawning in tanks is that the anaesthetic may be used more economically. The sex ratio for induced propagation is 2 females to 1 male, respectively. Males of small body weight and females spawning for the first time are preferred (Horvath et al., 1984) Anaesthesia Fish are generally anaesthetized in a solution of MS 222 (3-aminobenzoic acid ethyl ester) at a dilution varying from 1:5,000 to 1:20,000 (in practice, a solution of about 1: 10,000 is usually found satisfactory). Fish should remain anaesthetized for a minimum of time and only as deeply as necessary for the procedures involved. Gill cover movements should be monitored, oxygen should be provided since deficiencies can occur when many fish are kept in the same water. If one finds it is necessary to keep fish in the anaesthetic for longer time periods then another tank with normal water should be at hand into which the deeply anaesthetized fish can be transferred to recover. Fish are first marked to identify each spawner and coloured thread may be inserted into the dorsal fin. Marking is followed by weighing the individual fish since the weight is the basis of calculations for hormone treatment. It is advisable to plan the timing of the operations so that the spawners can receive the treatment when they are brought into the hatchery Hypophyseal hormone treatment Hypophysation is the traditional method of inducing fish to spawn and is widely practised in carp culture (Weil et al., 1986). Fresh, frozen, or acetone-dried pituitaries are obtained as a valuable by-product of fish processing. They are ground down, hydrated with fluid, (usually saline) and the supernatant injected into the broodstock on a body weight basis. Pituitaries are usually obtained from other cyprinids, predominantly the common carp. Experience has shown that induced propagation of carp is more effective if the hormone is administered in two doses. In the first treatment, 8-10 % of the total dose is given to bring the eggs into the stage of pre-ovulation. Then the second dose induces ovulation. When only one pituitary treatment is used, mg of dried pituitary is injected per kg of body weight. When two treatments are used the dose is somewhat higher. Suture of the genital orifice of females immediately after the second injection has been practiced (Billard, 1999), but proper monitoring and observation of fish behaviour renders this practice unnecessary. The solution is injected into the dorsal muscle of the fish. Fish would generally be anaesthetized before injection. The use of desoxycorticosterone acetate in the artificial The EFSA Journal (2008) Annex I, 40-81

69 spawning (hypophysation) of fish has been stopped because of harmful side effects, such as infections under the skin following injection. Such side effects are not noted with pituitaries Stripping and egg fertilization Extra care should be taken at this stage as the adults are susceptible to physical damage, slime removal and scale loss. Gametes, especially with the females are free flowing and much care needs to be exercised to prevent accidental loss of sex products. No water should be allowed to come into contact with the gametes as the eggs will instantly become sticky and cause clumping. Spawners therefore, are dried with a cloth before stripping, and eggs of each spawner are collected in separate containers. The weight of moist eggs is measured after stripping and from this number of eggs may be calculated. This will serve as a basis for further calculations (Horvath et al., 1984). In central Europe, 5-6 kg female Carp will produce on average 700,000 eggs (Billard, 1999). It is desirable to use the milt of two or more males during fertilisation of the eggs of one female. Sometimes the milt of one male is unfertile and in this case the sperm of the other male used will fertilize the eggs (Horvath et al., 1984). Milt is collected with the help of a pipette from anaesthetized males, as well as free from water and in measurable quantity. The sexual products stripped from the fish are mixed in a plastic bowl in a ratio of 100 eggs: 1 milt, respectively. After mixing thoroughly, a fertilizing solution is added. This solution is the same as that used by Woynarovich and contains 10 l of pond water, 40 g salt and 30 g carbamide (Horvath et al., 1984). This solution which prevents egg agglomerating (clumping) added at 10 times the egg volume and is stirred thoroughly for a few minutes with a plastic spoon. During this period the egg stickiness is eliminated but sperm are activated and fertilisation of eggs takes place. The eggs then begin to swell. The formation of peri-vitalline space begins. During the swelling period the fertilisation solution is added in small quantities and stirred slowly. A sudden addition of the solution results in clogging or matting of the eggs. Extra sperm and the protein dissolved gradually from the surface of the eggs are poured out and replaced by fresh solution. After a few minutes the eggs no longer adhere to one another (Horvath et al., 1984). Spawners should be kept undisturbed between the treatments and ovulation. Any stress affecting their nervous system may hamper ovulation. Maximum quiet, protection and constant temperature should be maintained until stripping. In an undisturbed environment carp will spawn in the tanks. The spawning will take place with loud splashing. If one male is placed with the females, it will choose the ripest female and start the spawning with her. Sometimes spawning is simulated even when no male is present. As the discharge of eggs is prevented by the suture, stripping should be started only after min of vigorous spawning activity. Fish removed from the tank should be those spawners showing most active spawning activity allowing others in the tank to complete ovulation. Spawners should be anaesthetized again before stripping. This is very important because loss of eggs during stripping will be less and the spawners will not be injured. After stripping, spawners should be placed into recovery ponds without delay to prevent further injuries On-farm movements On-farm movements are movements of fish within the aquaculture facility tend to short term in nature usually lasting less than 30 min. Because of the temporary nature of the activity, welfare issues are generally limited to physical damage (i.e. contact with nets, sides of The EFSA Journal (2008) Annex I, 41-81

70 transport vessel, etc.), dissolved oxygen content of the transport water, nature and levels of suspended solids and temperature shocks experienced when transferring the fish from one water body to another. Other water quality factors such as NH 3 content, ph and CO 2 are not usually a welfare issue. Berka (1986), Berka & Hartman (1991), and Wedemeyer (1996) comprehensively review the various methods in use for aquaculture along with detailed discussions regarding the biological aspects of fish transport. For short transport distances and times (>30 min) open tanks with aeration can be used. For longer times tanks are enclosed, aerated, and completely filled to prevent fish injuring themselves. Tanks are best emptied through an outlet hopper which can be attached to a hose. At temperatures above 15 C low doses of MS 222 (3-aminobenzoic acid ethyl ester) can be used to tranquilise the carp (e.g. 1:50,000 for common carp) and reduce movement and respiration (Horvath et al., 1984). Use of anaesthetic can increase the mass of fish transported but careful monitoring is required. During on farm transport operations, it is common practice to add low concentrations of NaCl to the transport water in order to minimise stress and manage associated osmoregulatory effects Sorting and Grading Sorting and grading happen at different times in the production cycle. Polyculture is widely practised in European carp culture and, after being removed from the pond, the fish are placed onto sorting tables where the individual species and size groups can be separated. Most of this separating and sorting is done by hand although increasingly, the fish are graded using mechanical graders, which tend to cause less damage. Such mechanical graders process the fish in water and prevent them from drying out. Potentially, it is during this phase that the most damage may be done to the fish. Contact with nets, hard surfaces and machinery can cause physical damage along, with the possibility of crushing and asphyxia. Operations should be carried out quickly and carefully to prevent damage to the fish. Collected fish are then weighed and transferred to the transport vehicle ready for dispatch to the over-wintering or marketing site (Horvath et al., 1992) Monitoring This section, although included under the management heading, is mainly relevant to water quality. Frequent monitoring of the water quality is essential as there are a number of variables that affect the well-being of fish. In culture systems, the main factors that need to be monitored are temperature, dissolved oxygen, ph and the metabolic by-products NH 3 and NO 2. These important parameters have to be maintained within certain limits if the fish are to survive and thrive. Consequently, regular monitoring and recording is vital if potential problems are to be avoided and trends in water quality determined. Depending on the culture system used, other parameters that need monitoring may include alkalinity, PO 4, total phosphorus, NO 3, CO 2, Biochemical and Chemical Oxygen Demand (BOD, COD), and turbidity. In addition to water quality, information is also needed on feed rates, growth, condition, mortalities, disease status and ultimately survival rates. These data enable the farmer to make informed husbandry decisions and ensure the continued health and welfare of the fish. The EFSA Journal (2008) Annex I, 42-81

71 Staff training on welfare To be successful and to maintain welfare standards in carp culture, it is important that staff at each unit is experienced and proficient. Staff recruitment onto fish farms is from both a qualified and an unqualified pool. Additional post-employment training occurs, either by attendance at organized courses or more usually by mentoring i.e. working alongside a more experienced member of staff. Husbandry staff awareness of the causes, signs and effects of stress on fish are vital as are the measures needed to reduce or remove the stressor. Failure to invest in the training and development of staff can lead to fish being subjected to avoidable stressors such as over-crowding, poor handling, underfeeding, sub-optimal culture conditions and inappropriate disease treatment. The concept of Good Stockmanship (MacIntyre and Turnbull, 2007) should be developed by investing in training and staff development Genetics Quality breeding programs exist for common carp. Many varieties and strains of scaly or mirror carp (with some large shining scales), including hybrids, are available. Artificial reproduction of carp is the basis for any breeding activities, during which farmers will intentionally pick up breeders with given phenotypes and/or genotypes. The numerous varieties of common carp have developed through a combination of forces, including geographical isolation, adaptation, accumulation of mutations and natural as well as human selection pressures. Crossbreeding and introgression played a further role in the development of various varieties, mainly through transplantation of domesticated European varieties into other countries (Hulata, 1995; Jhingran and Pullin, 1985). Live gene banks of common carp have been established in Hungary (Bakos and Gorda, 2001), in the Czech Republic (Pokorny et al., 1995), in Poland (Irnazarow et al., 1995) and in Russia (Katasonov et al., 1995). Differences among the European strains (land races) are limited, perhaps as a result of inbreeding (Kirpichnikov, 1981). Genetic improvement through uncontrolled selection has been practised in Europe for hundreds of years. This has led to the development of various local breeds (Schaperclaus, 1961; Moav and Wohlfarth, 1976; Moav, 1979). Selective breeding, consisting of isolating genetic combinations or mutants for morphological traits (body coloration and shape), crossbreeding and selection, has led to the development of many fancy carp varieties. Controlled selection experiments aimed at improving specific quantitative traits, performed in a way that permitted estimation of the magnitude of genetic gains, have been carried out only with the common carp. Research would be necessary to determine if genetic selection for one trait could affect other life history traits and have a negative welfare impact. Common carp is a domesticated species that well adapted to the husbandry systems within which it is reared Impact of diseases on welfare Disease is one of the major welfare issues in all fish husbandry. In the case of carp it is particularly related to environment. Most carp pathogens are facultative pathogens present in the environment. Those diseases with chronic, often sub clinical effects are often of greatest welfare significance. In the case of more acute conditions, control or treatment measures may have significant welfare impact in their own right. Good husbandry should be the major means of disease control. The EFSA Journal (2008) Annex I, 43-81

72 Transmission of ectoparasites causing a welfare issue is not relevant to the egg stage. Transmission of parasitic and fungal infection is possible either from the adults or from the water column if filtration is inadequate. During the process of hand stripping, mucus and scales may contaminate the gametes and be introduced into the incubation system. These ectoparasites cause no problems during the egg incubation stage but can significantly affect the newly-hatched larvae. Correct hygiene procedures are necessary to prevent vertical transfer of pathogens. There are large numbers of pathogens potentially affecting carp. This is especially true for parasites. In this report, only selected diseases of cultured common carp were reviewed. The diseases included in the report are considered to be of potential significance to carp welfare because of their: i) severity of effect on physiological integrity of fish; ii) known frequency of occurrence in farming systems; and iii) impact of preventive and curative measures. Most of the pathogens of common carp are facultative pathogens. They are almost always present in the water surrounding the fish, but they will cause disease only under certain circumstances. The theory of Snieszko (1974) on the primary role of environmental stress in the outbreak of fish diseases is especially important in warm water aquaculture, including carp culture, where mainly surface waters are used and the basic water quality parameters are subject to a wide range of fluctuations, as well as where the level of management is generally low. Several diseases of carp are typically stress-mediated : certain parasite infestations (costiosis, trichodinosis), bacterial gill disease, flexibacteriosis and spring viraemia of carp. For a better understanding of the role of environmental stress factors in an outbreak of fish diseases it is essential to study the response of the fish. In the scheme suggested for the stress response of fish (Peters, 1979; Mauzeaud and Mauzeaud, 1981) the most important physiological and biochemical changes occurring at the primary, secondary and tertiary levels were summarised. Certain of these changes can also be employed to detect disease at early stages or sub-lethal effects of environmental contaminants. A summary of the physiological tests for stress assessments of salmonids was published by Wedemeyer and Yasutake (1977). A similar system for silver carp (Hypophthalmichthys molitrix) was presented by Bejerano (1984). Data are available on the normal ranges or values of some of these parameters for common carp (Svobodova, 1987). The limits of the normal values of these parameters in fish can only be overcome by a description of the typical changes under the effect of different environmental factors, compared with the changes in nontreated groups. For the assessment of the effects of environmental stress on common carp a system of clinical diagnostic parameters was set up and tested (Jeney and Jeney, 1986, 1987; Jeney et al., 1992 a and b). Using this system, different environmental stresses of both natural and anthropic origin were investigated, typical changes (increase or decrease, compared with the control) in these parameters were presented. It was shown, that most of the natural and anthropic environmental factors studied, even though typical for normal technological conditions, caused marked changes at all three levels of stress response of the carp Parasitic diseases: White Spot (Ichthyophthirius multifiliis) disease Representatives of almost all major systematic groups of parasites have been found in carp. Altogether 226 parasite species were described (Landsberg, 1991). Environmental stress appears to play a major role in the development of epizootics caused by parasites of carp. This is especially true for ectoparasites, which may typically induce high mortality rates in handling facilities where fish become overcrowded, such as in over-wintering ponds or in densely populated growing ponds and reservoirs (Paperna, 1991). Other environmental The EFSA Journal (2008) Annex I, 44-81

73 factors (e.g. oxygenation, toxic ammonia, etc.) may also favour epidemics caused by ectoparasitic protozoa. White Spot (Ichthyophthirius multifiliis) Disease Ichthyophthirius multifiliis is a ciliated protozoan which invades the epithelia of the skin and gills of a wide variety of freshwater fish species world wide (Wahli and Matthews, 1999). In carp, the parasite causes a disease known as "Ich" or "white spot disease" and is a serious problem to commercial carp production (Matthews, 1994). The disease is highly contagious and spreads rapidly from one fish to another. An outbreak, if left untreated, may result in very high mortality depending on the degree of infestation and other factors. All age groups are susceptible and disease occurs between 3 and 28 C (Schlotfeldt and Alderman, 1995). Disease description The infection results in small white spots and blister like lesions on the skin or gills. Prior to the appearance of lesions, fish may show signs of irritation, rubbing and flashing, weakness, loss of appetite, and decreased activity. Infected gills will be pale and swollen. Diagnosis is easily confirmed by microscopic examination of skin and gill lesions. Treatment Control of I. multifiliis is only achievable on free-swimming stages (tomites) that are susceptible to chemical treatment. This means that application of a single treatment will kill tomites which have emerged from cysts and have not yet burrowed into the skin of host fish. Repeated treatments (until all mortality from I. multifiliis has stopped) are needed to control an epidemic. Common chemicals used to treat include copper sulphate, copper-oxy-chloride, formalin, and potassium permanganate that are all effective against I. multifiliis. Currently, none of these compounds are allowed to be used in food fish. As an example, a bath of 250 mg formalin /l for 30 to 60 minutes (followed by a water change) is recommended to treat fish. Sick fish may be unable to tolerate a full treatment. A bath of formalin, long term, can be used in a tank system at a concentration of 15 mg/l and does not need to be flushed out. Salt can also be used to control infections in small volumes of water. This is not practical in ponds because even a light salt solution of 0.01 % (100 mg/l) would require large quantities of salt. In small volumes (i.e. tanks), however, salt can be useful. Fish can be dipped in a 3% (30 g/l i.e. 30,000 mg/l) solution for thirty seconds to several minutes, or they can be treated in a prolonged bath at a lower concentration (0.05 % = 500 mg/l). Salt at low concentrations (0.01 to 0.05%) is an excellent means of controlling I. multifiliis in recirculation systems without harming the biofilter. An ultraviolet filter is recommended as an aid in preventing the spread of the parasite in a recirculation system Fungal diseases: saprolegniasis Fungal infections of common carp are serious problems of both natural fisheries and intensive aquaculture. Fungal infections are also a persistent problem in warm water hatcheries as any dead eggs quickly become a focus of proliferation which can than spread to adjacent healthy eggs. In spite of their importance, our knowledge about the fungal infections is still poor, for two basic reasons: difficult identification of pathogenic fungi (Pickering and Willoughby, 1982) and the prolific growth of saprophytic fungi once fish are dead (Willoughby, 1971). The potential fish pathogens of the family Saprolegniaceae were reviewed by Pickering and Willoughby (1982) (Table 2). The EFSA Journal (2008) Annex I, 45-81

74 Saprolegnia spp., Achlya spp. and Branchiomyces spp. are probably the major pathogenic fungi in the common carp. Here we give a short description of the genus Saprolegnia, as well as saprolegniasis of common carp, the disease caused by them. Saprolegniasis The genus Saprolegnia is characterised by the production of biflagellate zoospores which swim away after emptying of the zoosporangia. New zoosporangia often form in the old ones. Saprolegnia parasitica Coker (in Willoughby s system of classification syn. Saprolegnia diclina Type 1) is most frequently associated with fish, and produces sexual organs only in special cases. Zoosporangia are 0,3-0,6 nm long, cylindrical, often irregular in shape, and appear on the 2 nd - 3 rd day of culture. Ripening and release of zoospores soon begins. The zoospores are spherical with two flagella, motile and 10 pm in diameter. Disease description Gross pathology of Saprolegnia infection is characterised by conspicuous fungal colonies growing on the body surface of the fish. These cotton-wool-like lesions are normally white in colour, or discoloured by the accumulation of debris between the fungal hyphae or as a result of a simultaneous bacterial infection. The fungus can colonise almost any area of the external surface of the fish. Once infected, fish do not normally recover from saprolegniasis unless treated. Death of the fish is due to massive osmoregulatory problems caused by destruction of the superficial tissues over large areas of the body surface although the survival time is influenced by the precise location of damaged tissue. Saprolegniasis has been considered to be a secondary condition with fungal hyphae normally colonising existing lesions on the fish. Although fungal infections are often secondary to other diseases and to physical damage, there is also evidence that Saprolegnia diclina Type 1 (syn. S. parasitica) can also act as a primary pathogen in undamaged, healthy fish (Pickering and Christie, 1980). The following conditions can increase the susceptibility of fish to infection: wounds are potential sites for Saprolegnia colonisation; physical damage (Tiffney, 1939; Egusa, 1965); high stocking density; any environmental conditions and manipulations that result in physical damage; sexual maturation; other infections, especially those that cause ulceration of, or damage to, the superficial tissues of the fish; or cause a stress-mediated increase in plasma corticosteroids (Nord et a1.,1977; Neish and Hughes, 1980). Treatment Malachite green has been a treatment of choice for Saprolegnia infections during all stages of the life cycle of carp and other commercially produced fish species (Alderman, 1985, 1991). Formalin stabilized chlorine dioxide was suggested as a control agent for fungal infections, first of all saprolegniasis (Hiney and Smith, 1993). General measures to improve water quality should also be considered Bacterial diseases: motile Aeromonas septicaemia Review of diseases of carp shows relatively small number bacterial pathogens (Jeney and Jeney, 1995). Motile Aeromonas septicaemia Motile aeromonads are common and ubiquitous members of fresh water ecosystems, and can be part of the microbial flora of aquatic animals. They may be pathogens of poikilotherms, homeotherms and even man (Fraire, 1978; Salton and Schnick, 1973). Motile aeromonads show very considerable heterogeneity and their taxonomy is unclear. This group comprises several species: Aeromonas hydrophila (syn. A. liquefaciens), A. sobria and A. caviae (syn. The EFSA Journal (2008) Annex I, 46-81

75 A. hydrophila subsp. anaerogenes). Of these species, A. hydrophila is of great importance because of its potential impact on carp culture (Roberts, 1993). Although motile aeromonads may occur in relatively pristine waters, they are much more abundant in waters with a high organic load (Hazen et al., 1978). Because the normal conditions of a carp-rearing pond are close to these, and Aeromonas hydrophila is a normal inhabitant of this environment, carp are constantly exposed to infection. Disease outbreaks are common when carp are under stress from crowding, low oxygen, high temperatures, etc., and significant losses from such outbreaks occur annually. Disease description Clinical signs of the disease are rupture of minor blood vessels and haemorrhages caused by haemolysin, which may be associated with ulcerative skin lesions. The size of external lesions may vary. The ulcers are usually shallow. Secondary infection of ulcers by fungi is common. In carp the condition may be pre-acute, with few signs, acute, with the typical syndrome described above, or chronic with large, long-standing ulcers. It is often associated with abdominal oedema or dropsy. Internally the principal feature is hyperaemia of the viscera with haemorrhage over mesenteritis and within the visceral and parietal peritoneum. There may be an excess of clear or reddish ascitic fluid in clinical dropsy. The spleen and kidney are enlarged. Treatment Control of A. hydrophila infection should be linked to the control of the associated factors which have contributed to infection of the host. However, when an outbreak occurs, it is very difficult to determine the underlying stress factors or primary infections and it is not possible to change water flows or stocking densities with any ease. Thus treatment is limited to the use of antibacterial compounds in the feeds. Besides development of antibiotic resistance (Mitchell and Plumb, 1980; Chang and Bolton, 1987; Ansary et al., 1992), the efficacy of antibacterial treatment is lowered due to the loss of appetite in diseased fish. Efforts to develop vaccines against MAS have not been successful for long time, mainly because of the wide serological diversity among A. hydrophila strains Viral diseases: spring viraemia of carp In the literature on fish viruses and viral diseases 23 viruses were isolated from cyprinids. Two of them are from common carp: Rhabdovirus carpio (causative agent of spring viraemia of carp, Fijan et al. 1971) and Herpesvirus cyprini (causative agent of carp pox). This report highlights SVC for purpose of investigating welfare related issues. Spring viraemia of carp (SVC) is an acute haemorrhagic and contagious viral infection of the common carp in Europe. The isolated virus (SVCV Rhabdovirus carpio) proved its aetiological role in SVC. Disease description SVC virus has the characteristics of Rhabdoviruses and the agent is pathogenic to carp of all ages. The disease becomes manifest when the water temperatures rise in the springtime. Moribund fish show dark colouration, low respiration, exophthalmia, inflamed and oedematous vent, pale gills and haemorrhages in the skin. Internally there are frequently haemorrhages in the viscera and swim bladder, and peritonitis with serous or haemorrhagic exudate is mostly present in acute cases. A clinical diagnosis of SVC is possible if serious mortality occurs among carp during spring or early summer and affected specimens show the key features of the behavioural changes and the above-described signs. For confirmative The EFSA Journal (2008) Annex I, 47-81

76 diagnosis the Rhabdovirus carpio should be isolated and identified serologically, or the viral antigen should be identified serologically in tissue sections. Treatment Theoretically there are 5 basic control measures for SVC: avoidance of sources of virus; development of specific-pathogen-free (SPF) broodstock; temperature manipulation (rearing fish above 20 C); genetic selection for resistance to SVC (Kirpichnikov et al., 1972); and immunoprophylaxis. Practically all these control measures have their limitations: no methods to detect carrier state, impracticality of control, lack of methods of chemical control, and quality problems with the only tested SVC vaccine (Tesarcik et al., 1984). Research on a recombinant subunit vaccine against spring viraemia of carp aimed at the production of a low-cost, completely safe and effective vaccine could provide a possible solution (Rossius and Thiry, 1993). Swimming carp fry are particularly susceptible to skin damage associated with predation and to infection with ectoparasites, which may cause mortality or chronic disease. There are no approved methods to treat carp at this stage. If pond preparation and the technology of fry nursing are not carried out correctly fish may suffer malnutrition or starve, which results in an increase in ectoparasitic infections. Larvae may also be predated or damaged by large zooplankton. If disease problems arise it is very difficult to apply any treatment due to the size of the ponds and the short duration of the nursing period. If robust and healthy fry are stocked into well prepared fingerling ponds which are properly maintained there will be no major disease problems. If pond management breaks down then disease, mainly caused by ectoparasites may occur. Disease treatments in relatively large fingerling ponds are extremely difficult and expensive and it is therefore better to prevent problems arising through good pond management. For on-growers, the application of bio-security systems to pond production offers a number of challenges. The open nature of the ponds, interaction with the environment and the source of water all make 100% protection unachievable. Diseases can potentially be transferred by infected fish entering pond, transmitted by birds and animals or enter the pond directly in water (suspended spores, e.g. in case of moulds). Through these pathways, carp may become exposed to different diseases (SVC, KHV). However, effective, efficient and well-run rearing units should make all possible efforts to develop and implement those biosecurity measures that are feasible to protect the health of their stocks. Where fish are to be transferred to other ponds, crowding may trigger infections which will subsequently manifest themselves. Harvested fish are transferred to winter/storage ponds and mixed with fish coming from different locations thus potentially allowing transfer of diseases. During the sorting and separation process, opportunities arise to mitigate some of the disease problems which may be observed in the monitoring process on those fish not going to the market. Before transport operations, only NaCl solution is available to eliminate ectoparasites (protozoa). Sudden change of the water salinity requires a response from the osmoregulatory system (Abo Hegab and Hanke, 1982; Gupta and Hanke, 1982). Marketable fish, High stocking densities normally enhance the transfer of ectoparasites between fish. The temperatures at which marketable fish are maintained, however, are such The EFSA Journal (2008) Annex I, 48-81

77 that despite possible slow healing of occasional traumatic lesions there is no significant welfare issue associated with infectious diseases in storage ponds. Apart from occasional protozoan parasite infestations and the effects of low ph, acid snow melts, there are few disease problems during the over-wintering period. Normally overwintering fish would not be seen to be moving around in the pond. If fish are disturbed and seen to be active around the water inflow, this would indicate a possible health problem (e.g. gill infestation). Before stocking, spawners injured during hatchery work should be treated or sorted out. During treatment, spawners should be held for a few days either in tanks with good water supply, or in small quarantine ponds where they can be monitored, treated and fed with specially medicated feeds rich in vitamins, proteins, etc. Quarantine is especially important for those breeders which have not spawned for some reason. As a result of some vital process impairment, hormone-treated fish can perish easily under the more adverse circumstances prevailing in ponds. If possible these fish should be replaced. This will have a beneficial effect on selection of broodstock which will tolerate conditions of induced spawning. During the selection process spawners selected should be immersed in a 2-5% salt solution for a few minutes to remove external parasites. At the start of wintering period and again at its end in early spring it is advised to feed fish with medicated feeds containing antibiotics at appropriate doses Disease control measures Biosecurity Biosecurity may be defined in many ways and in the aquaculture context its technology is still evolving. The biosecurity concept covers implementation of a set of programmes and procedures preventing the entry, establishment or spread of unwanted pests and infectious disease agents whether they are a risk to humans, animals, plants or the environment. Biosecurity is the state of having applied appropriate measures to prevent or limit the possibility of pathogens entering populations from an exogenous source. It may be applied at the regional, national, or farm level or between particular holding facilities. Biosecurity measures involve national and international controls, disease surveillance and border controls, as well as controls relating to the farm and its immediate surroundings. It invariably requires disinfection applications, husbandry disciplines and good record keeping. A particular requirement, often recognised solely in the breach, is disinfection of transportation equipment both before and after transportation of fish (Danner & Merrill, 2006). Although biosecurity controls are increasingly being applied in aquaculture and by preventing disease outbreaks have significant welfare significance, currently, they are hindered in many areas, by the lack of understanding of the principles, lack of enforcement, and failure to understand the risk basis upon which they are applied. Also the degree of discipline they require in their application are somehow inimical to many farmers and invariably enhancement of biosecurity can only be induced following direct example of benefit after a serious disease outbreak. Increasing awareness of the risks associated with the movement of live fish, internationally, including aquarium fish, has led to concern for improvements in biosecurity at international and national levels, at farm level there is still great need for training and establishment of robust biosecurity arrangements that will be both applied and monitored. Currently, however, there is a lack of adequate information on the efficacy of the various disinfectants used in terms of the fish pathogens, and in particular the The EFSA Journal (2008) Annex I, 49-81

78 toxicity of many of the disinfectants used both in relation to the fish and the environment. A start has been made to resolving these issues (Scarfe, 2006; Graham, 2007), but inadequate knowledge and application of biosecurity is still a significant factor in the overall assurance of welfare of farmed species Monitoring mortalities / survival rates Council Directive 2006/88/EC contains obligations to report "increased mortality", however most carp farms do not currently have any formal means to differentiate between expected mortalities and unexpected or increased mortalities. Presence of a named Veterinary Surgeon and regular and detailed Veterinary audit are important to the management of diseases and support welfare as well as health. But currently such facilities do not exist in European carp culture. Mortalities of fish during the production cycle can result from a variety of causes, including, disease, predation, damage, and adverse environmental conditions. Since any population of animals suffers from mortalities it would be unreasonable to aim for no mortalities. At present there is no data for carp farms as to what level of mortalities are experienced in the various farming systems or what level of mortalities might be considered acceptable. Very poor welfare (e.g. disease, poor growth and mortalities) is not cost-effective for the farmer, so even the farms that have relatively poor fish welfare have found a balance between welfare and economic productivity. However, in many cases high or increasing mortalities are an indication of disease problems with serious economic and welfare implications. At present many farms rely on the experience of the farm manager to decide when mortalities require additional action. This is not a simple task since mortalities vary over time depending on a variety of factors such as life stage, temperature, farming system, presence of endemic diseases and others Drug usage Carp diseases are a significant welfare hazard but currently very few of the treatments which are effective are used due to the fact that these veterinary medicinal products are not authorised. Chemicals/drugs used in pond culture are regulated by the EU and each member state. Their use, however, is very low, due to the predominance of extensive production systems. Because the large ponds are very large ( ha) the stock (often exceeding 1,500 kg/ha) cannot be treated effectively. Thus, prevention remains the only solution. The most recent infectious disease outbreak has been Koi herpes virus. One solution to avoid serious loss from a sudden disease outbreak is to diversify production. The appropriate use and control of chemicals in farming activities is a legal requirement. Detailed records therefore need to be kept for any chemical treatments whether they are for fish disease control, weed control or other purpose. In addition, most chemotherapeutics have a minimum withdrawal period (MWP) or a maximum residual level (MRL) of the active compound in the flesh of the fish, which are important considerations when the fish are intended for human consumption. Chemicals to treat disease should be used with caution and the chemical treatment should not be administered without a proper diagnosis. Most chemical treatments are harmful to the fish in some way and if administered incorrectly can actually do more harm than good. Several factors need to be taken into consideration when choosing a treatment. These include the species of fish, the system in which the fish are held and the route of administration. The EFSA Journal (2008) Annex I, 50-81

79 Applications of chemical treatments, the capture and the preparation for treatment induce stress in the fish. There are five major routes by which fish are exposed to chemotherapeutics: waterborne, oral, injection, spray and swab. Waterborne. This is the most common method used in fish culture system and has the obvious advantage to reduce or avoid handling of the fish. However, not all chemotherapeutics are water-soluble and hence not all can be administered this way. The chemicals can be administered by prolonged immersion, bath or flush through. Prolonged immersion. To avoid any handling of the fish the chemical is added to the system. It is mostly suitable for the treatment of external pathogens such as skin and gill parasites, fungi and skin bacterial lesions. However, delivered drugs are usually toxic to a wide range of organisms. They can therefore be problematic in recirculating systems and filtered aquaria where the biological filter bacteria are likely to be affected, also in open water extensive growing ponds where the live food that is essential for the productivity of these ponds will be affected. Copper treatments, for example, are highly toxic to certain aquatic invertebrates. In extensive systems, which usually contain large volumes of water; this means realistically that chemical immersion in extensive systems is hardly applicable. Bath. This is usually the cheapest, most effective and commonly used way of treating fish. It allows a precise dosage to be given for a controlled time period with greater control over the fish themselves. However, bath treatments imply the initial capturing of the fish. For carp, farming system will often require netting of the stock. Since bath treatment will obviously have no effect on any pathogens or their stages that occur in the water or in intermediate hosts, then repeat administration may be required. Flush. This technique is particularly relevant where fish are held in systems that have a continuous, high water flow-through. A given quantity of the chemical is added at the tank inlet and allowed to flush through the system. The efficacy and efficiency of this technique depends on timing of the chemical release and uniformity of its dispersion. In addition, reactive fish may avoid the chemical flash, and hence receive suboptimal exposure. Although this method of chemical administration is not really suitable for most carp farming systems the technique is routinely used in the treatment of eggs held in Zuger jars. Oral. This may be the ideal way for the administration of some chemotherapeutics. Generally, oral treatment takes place after a 24-hour period of starvation and the fish should be fed at 2% body weight. The dosage should be calculated to give an adequate dose to any fish that eats at least 1% of its body weight day. To work effectively the correct amount of treated food should be consumed by each fish. This is unlikely to happen however as infected fish may lose appetite and dominant fish may eat more than expected. In addition, young fish may eat only live food. However, novel delivery techniques are being developed, for example fish can be fed on Artemia that has been impregnated with chemotherapeutics prior to delivery, and drugs can be encapsulated to increase the efficiency of the delivery in the fish gut. Injection. This is the best means of delivering the correct dose of therapeutic individual fish. Obviously it requires handling, possibly anaesthesia, and is therefore extremely stressful for the fish. This technique should be performed by skilled personnel. The recommended sites for most injectable drugs are either into the peritoneum (intraperitoneal) or the muscle (intramuscular). Spray. Some drugs and vaccines can be sprayed onto the skin or gills of fish and this can be conveniently carried out during routine husbandry procedures such as grading. The EFSA Journal (2008) Annex I, 51-81

80 Swab. Some treatments may be given topically to the affected area. This is particularly useful when treating large, expensive fish exhibiting bacterial skin lesions. Although the fish may respond to a systemic antibiotic, the lesion may take time to heal and in the meantime will have significant impact on the health of the fish, particularly in relation to secondary infection. A broad spectrum biocide is usually applied to all areas of the lesion and after 30 seconds the area is sealed by the application of a water-repellent substance such as Orabase TM or Vaseline TM. The selection and dose of any chemical or drug is dependent on a wide range of variables including the method of administration, the disease, fish species, age of fish and environmental parameters. Some typical treatments are listed in Hoole et al., There is a wide range of drugs being used in aquaculture worldwide. The regulations are different on different parts of the world. In one of the recent reviews Schnick et al., 2005 gave a detailed list of drugs and vaccines that are used or planned to be used in all the major aquaculture regions, including Europe. Four categories are differentiated: 1. Drugs approved for aquaculture in the world; 2. Vaccines licensed for aquaculture world-wide; 3. Priority aquaculture drug needs in each country or continent; and 4. Priority aquaculture vaccine needs in each country or continent Vaccination As with any animal husbandry system, the intensification of fish farming has inevitably resulted in the emergence of disease problems, infectious diseases in particular. Carp farming is still to a large extent extensive, but in the case of Koi carp, for example, the value of the commercial product is now recognised as being worth treating with more expensive antibiotics or vaccines. Since the establishment of intensive fish farming as an industry, antimicrobials have been used for fire fighting of epidemics in order to keep disease problems at an acceptable level, but have latterly been superseded by development if vaccines. In carp farming however, this stage has generally not been reached (Fijan, 1988) and selective breeding for robustness and disease resistance, has been the norm rather than use of antibiotics and vaccines. Although one vaccine for use by intraperitoneal injection in oil emulsion, against spring viraemia (SVC, Spring Viremia of Carp) was marketed in Czech Republic (former Czechoslovakia) with positive results (Tesarcik and Macura, 1988) it is not licensed for use in carp in the EU. In fish, killed vaccines are generally used. Killed vaccines are based on growth of a given pathogen in culture followed by inactivation, usually by means of formalin. Most of the experimental vaccines against SVC were based on this principle. But Fijan et al. (1977) described use of a live vaccine under commercial conditions recent developments of vaccines against the Koi herpes virus (KHV) infection, a highly infectious and lethal disease which affects both Koi and common variants have used live attenuated strains. These are widely used in Israel and such fish are imported into the EU but no such vaccine is licensed for actual use in the EU. This would appear to be an area where biosecurity could be compromised. More sophisticated, killed vaccines against KHV are under development and are expected to be offered for licensing within a relatively short time, but again these are likely to be oil adjuvanted, which is a welfare concern. Carp may be exposed to killed vaccines by immersion, as a component of the diet or by injection. The majority of current candidate vaccines are, of necessity, applied by the injection route. In welfare terms and in terms of ease of exposure, other routes are preferable, The EFSA Journal (2008) Annex I, 52-81

81 (Baba et al., 1988; Daly et al., 1994) but, in most cases protection is limited unless injection, along with an adjuvant, is the route of administration. Adjuvants are widely used in vaccines to increase and prolong the immunogenic effect of the antigenic components of a vaccine. In fish vaccines, although aluminium hydroxide adjuvants may be used on occasion, the most frequently used adjuvants all represent modifications of Freund s incomplete adjuvant, water in oil emulsion, which causes a localised chronic inflammatory response at the site of injection, trapping the antigen and ensuring longer exposure to the macrophage and lymphoid elements of the immune response to it Methods of vaccination In most farmed species, where vaccines are employed they are given via a parenteral route, since adjuvants are usually required and this generally precludes other routes. Vaccination cannot be used in very small fish which are not yet fully immunocompetent, or able to tolerate the volumes of antigen necessary. Vaccination by injection is generally into the peritoneal cavity. In potential brood fish, the adhesions induced by the adjuvant may cause major clinical effects on the developing ovaries and testes and, significantly, limits fecundity. In such fish, vaccination is usually performed intramuscularly into the dorsal median sinus, which of course renders them unsuitable for human consumption. Immersion vaccination, where it is feasible, may be carried out by direct immersion, or by the so called shower method in which the vaccine is sprayed onto the fish. The immersion method may induce an effective immune response in fish and an advantage of the method is that a large number of fish may be vaccinated at the same time with a minimum of handling. Fijan and Matasin (1980) demonstrated good results with immersion vaccination against SVC in carp fry but the higher dose levels required for such vaccination means that for economic reasons it is only economically feasible with very small fish. Incorporation of vaccines within the feed would be considered, a priori to have great advantages in that it can be administered to the fish without any handling stress. It depends however on how much food the individual fish consume, and most vaccines are denatured by the digestive tract or are poorly absorbed. Fijan et al. (1977) achieved good experimental; protection, with an oral vaccine given at the end of the year, but they used a live virus antigen and the work was not continued because of a lack of commercial feasibility Welfare and vaccination in fish The most important effect of vaccination in fish is that, provided other factors such as husbandry and welfare are adequate, it prevents disease outbreaks, reduces mortality considerably and reduces the use of medicinal products. Where vaccination is effective, a few fish will suffer from the disease it protects against, but the environmental loading of such pathogens is also reduced for other fishes, in the absence of outbreaks. In the case of bacterial diseases, in the salmonid farming industry, where vaccination has had the greatest effect, its introduction has dramatically reduced the use of antimicrobials and also modified the multiple disease resistance patterns of such pathogens, which were emerging. In carp culture however, the extensive nature of the industry has not yet led to demands for such vaccines. On a general basis, although, vaccination is proven effective in protection against many serious fish diseases, and this undoubtedly represents a major welfare benefit, there are also certain disadvantages to be considered. These are handling stress at vaccination, growth retardation, deformities in the vertebral column, adhesions in the peritoneal cavity. Stress The EFSA Journal (2008) Annex I, 53-81

82 associated with vaccination relates to the distress induced by the process of crowding and catching, the stress of anaesthesia, and the pain associated with the post-vaccination reaction. These are all very limited in the processes involved in oral or immersion vaccination, but where an adjuvanted vaccine is given by injection they may be considerable. 6. Risk assessment approach to welfare of common carp 6.1. Introduction Poor animal welfare problems are generally the consequence of, inter alia, poor management, inappropriate environmental conditions, disease and interactions thereof. Presently there are no standards for animal welfare risk assessment, but previous studies exist where risk assessment for animal welfare has been explored (Anonymous, 2001; EFSA, 2006). In this section, the application of risk assessment to the study of welfare common carp is described. Risk assessment is a systematic, scientific-based process to estimate the magnitude of and exposure to a hazard and includes 4 steps: hazard identification; hazard characterisation; exposure assessment and risk characterisation. In food risk assessment terminology (Codex alimentarius), a hazard is a biological, chemical or physical agent in, or condition of, food with the potential to cause an adverse health effect. The risk is a function of the probability of an adverse health effect and the severity of that effect, consequential to a hazard(s) in food. Making a parallel to the Codex alimentarius risk assessment methodology, a hazard in animal welfare risk assessment is a factor with a potential to cause a negative animal welfare effect (adverse effect). A risk in animal welfare is a function of the probability of occurrence and the consequences of occurrence. Four parameters were scored to assess the importance of a hazard: 1) the probability of a given target population to be exposed to a particular hazard has been scored as frequency of occurrence of the hazard; 2) the proportion of the population affected; 3) the consequences of exposure have been scored by severity of the effect in the individual; and 4) the duration of the effect. Mortality was additionally scored to provide more information on the consequences of the hazard. While hazards usually relate to negative welfare impacts, the risk assessment approach could be also extended to include positive welfare consequences (resulting in risk-benefit analysis). Factors which may result in improved welfare were not considered in this analysis. The degree of confidence in the final estimation of risk depends on the uncertainty and variability. Information obtained from epidemiological, experimental, and laboratory animal studies have a level of uncertainty, related to, inter alia, the number of animals used, frequency of observations and the test characteristics. Uncertainty is increased when results are The EFSA Journal (2008) Annex I, 54-81

83 extrapolated from one situation to another (e.g. from experimental to field situations). Uncertainty also arises from incomplete knowledge. Uncertainty can be evaluated (and reduced) by carrying out further studies to obtain the necessary data or quasi-formally by using expert opinion or by simply making a judgment. Variability is a biological phenomenon (inherent dispersion) and is not reducible. The importance of welfare hazards will inevitably vary between farms and countries and over time. Reduction in variability is not an improvement in knowledge but instead reflects a loss of information. However, it is not always easy to separate variability from uncertainty. Uncertainty combined with variability is generally referred as total uncertainty. The methodology described in this section was based on the approach used in the previous EFSA scientific reports on welfare of fish, Atlantic salmon and trout (EFSA-Q and EFSA-Q ). However, due to the number life stages of common carp in production systems, some changes were made. The final risk score used duration of the effect of the hazard, while in the previous reports duration of the hazard and duration of effect were used. In the present report, duration of the effect was scored as a proportion of the time span of the life stage under consideration (e.g. if the life-stage lasts 60 days and the effect of the hazard persists for 10 days the score was 1/6). In the previous fish welfare reports the denominator used was the total remaining life potential lifespan after the hazard occurred. It is therefore not appropriate to use the final risk scores to make comparisons of the importance of hazards between species Steps of risk assessment For risk assessment of welfare of common carp, Cyprinus carpio, the different production systems, as well as the different life stages were identified. The different life stages we used were: fertilised eggs, yolk sac fry, free living fry, nursed fry, fingerlings, on-growing and over-wintering carp, marketable fish, and broodstock (Table 2). The different production systems vary depending on the life stage and are summarized in Table Hazard identification Factors potentially affecting the welfare of carp were considered and this information was used to identify potential hazards. A list of potential categories of hazards to fish welfare and health of carp was drawn up with reference to the different life stages of the fish as well as to the different types of production systems. Different factors that may affect the welfare of farmed fish are for example, water temperature and stocking density. These factors may also more broadly be described as conditions that may have a direct impact on the welfare and health of carp. Subsequently, hazard (a detrimental factor) identification (clinical signs and physiological changes), its character, and the consequences of it occurring, are all important issues to be taken into account when making a risk assessment. The list of potential hazards was established by the working group. The tables (technical additional data appended to this report as excel files) were designed to cover the 3 stages of the risk assessment: hazard specification, hazard characterisation and exposure assessment. The EFSA Journal (2008) Annex I, 55-81

84 Hazards may directly affect an animal or indirectly by changing the animals environment so that their ability to fulfil their basic needs is diminished, which can also lead to animal welfare problems Due to the already complex tables we concentrated on single factors without interactions and on the negative effects. However, since production factors can interact and welfare problems are generally due to multiple exposures to different factors, any positive or negative interactions with other factors should be reviewed. Interactions and positive effects are described in the text if deemed necessary Hazard characterization The objectives of this step are: 1. to examine and describe the consequences of an exposure to a hazard; and 2. to assess the relationship between the level of the hazard in terms of frequency and duration and the magnitude and likelihood of the adverse effect occurring at population level. The severity of the adverse effect caused by the hazard is described and scored in the following ways. The score was based on scientific evidence, when available, or expert opinion on the level of physiological and behavioural responses. Table 3: Severity of adverse effect Evaluation Score Explanation Limited 1 No or limited pain, malaise, frustration, fear or anxiety as evidenced by measures of the normal range of behavioural observations, physiological measures and clinical signs for >95% of the species or strain/breed Moderate 2 Moderate changes from normality and indicative of pain, malaise, fear or anxiety Severe 3 Substantial changes from normality and indicative of pain, malaise, fear or anxiety. Very severe 4 Extreme changes from normality and indicative of pain, malaise, fear or anxiety, that if persist would be incompatible with life. A hazard is not only described by the severity of its adverse effect, but the proportion of the population affected likelihood of effect. Table 4: Likelihood of effect (proportion of population affected) Evaluation Score % of population affected by the hazard Very low Low Moderate High Very High The EFSA Journal (2008) Annex I, 56-81

85 The duration of the adverse effect, i.e. the consequences of the hazard, were assessed in days and converted to a proportion of the life stage when the hazard occurred for the calculation of the final score. A problem in scoring the duration of adverse effect arises when the animal dies as a consequence of a particular hazard. Death may not be considered as a primary welfare problem. If the adverse effect is fatal then the duration of the adverse effect in the period before the effect causes mortality is the key welfare issue. However, the population level of mortality might indicate a welfare problem. Mortality The percentage of the individuals affected by the hazard which are likely to die as a result of exposure to the hazard were scored (see Table 9). This parameter is not used in the risk estimate calculation. Table 5: Proportion of the population which are likely to die as a result of exposure to the hazard Evaluation Score % of population Very low Low Moderate High Very High Exposure Assessment Exposure was scored as the frequency of occurrence of a hazard during the life stage of the fish (Table 5). Table 6: Frequency of exposure Evaluation Score Explanation Extremely low 1 The exposure would be extremely unlikely to occur Very low 2 The exposure would be very unlikely to occur Low 3 The exposure would be unlikely to occur Moderate 4 The exposure would occur with an even probability High 5 The exposure would be very likely to occur The EFSA Journal (2008) Annex I, 57-81

86 6.6. Uncertainty The uncertainty value is an indication of the information is indicating the type of information available, that is whether there are different studies with differing conclusions, but also whether scientific information, published or unpublished, is available. A single combined uncertainty score (low, medium and high -Table 7) was given for the overall uncertainty of all the parameters. Table 7: Uncertainty score Score 1 Low Solid and complete data available; strong evidence in multiple references with most authors coming to the same conclusions 2 Medium Some or only incomplete data available; evidence provided in small number of references; authors conclusions vary from one to the other; Solid and complete data available from other species which can be extrapolated to the species considered 3 Max Scarce or no data available; evidence provided in unpublished reports, or based on observation or personal communications; authors conclusions vary considerably between them 6.7. Scoring process Experts were asked individually to complete the risk tables for each hazard in each life stage. For some life stages, separate tables for different production systems needed to be completed. The scoring was based on current scientific knowledge, published data, field observation and experience of carp farming. In general, a single expert initially completed tables for groups of hazards, and the results discussed and adjusted during a group discussion Risk characterization Risk characterisation integrates hazard characterisation and exposure assessment into a risk score. In the case of the fish welfare risk assessment that included a semi-quantitative risk score for each life stage in all of the production systems employed during this life stage. This step aims to estimate the likelihood of occurrence of the adverse effect in a specific production system at a specific life stage of the fish. It aims to give information to the risk manager to evaluate a specific situation regarding maximising good welfare. The risk estimate was calculated for each hazard, and expresses its animal welfare burden in the considered population. Risk score = (severity)*(duration of effect)*(proportion of the population affected)*(frequency of hazard) The scores of frequency of hazard, severity and likelihood of effect were standardized to give even weighting to the scores (frequency of hazard /5; severity / 4 and likelihood of hazard / 5). The risk score was multiplied by 100 to make it easier to read. The EFSA Journal (2008) Annex I, 58-81

87 This formula assumes the following: - linearity of the severity scores (2 days suffering from a score 2 effect is equivalent as 1 day suffering from a score 4 effect) - no interactions between the hazards - that the hazards are mutually exclusive Because the previous assumptions are not verified the risk scores have to be interpreted with caution. Secondly, the risk scoring is semi-quantitative. Thus the scores allow a ranking but do not give meaningful absolute figures (e.g. a risk score of 12 should not interpreted as being twice as important as a hazard with a score of 6). Uncertainty scores could not be used in the risk estimate directly but are provided in the tables as an indication of the robustness of the ranking. The score may also be used to highlight areas where further research is needed to improve the certainty of the scientific data. The risk assessment allows the relative importance of hazards in the same life stage to be assessed. Comparisons have been made between hazards in different production systems for the same life stage Discussion Introduction Risk assessment offers a systematic and defensible approach to comparing potential welfare hazards. The qualitative scoring system allows hazards within life stages to be ranked, however, comparisons between life stages are not appropriate. The scores need to be interpreted with caution. It was considered reasonable to use the final risk score to approximately rank hazards, but a more quantitative comparison may be misleading (i.e. a hazard with a score of 12 should not be considered twice as important as a hazard with a score of 6). An examination of the parameter scores (underpinning the overall risk score) provides an indication of why the hazard achieved a high score, and is needed to support recommendations to improve the welfare of farmed carp. One limitation of the approach adopted is that hazards were considered individually, and could not take into account interaction between hazards Stage specific discussion Eggs The important hazards for both Dubish ponds and jars were water quality parameters. The highest ranked hazards were low water oxygen content for jars and low water temperature in Dubish ponds. Too high or too low water flows were important in jars whilst only low water flow was important in Dubish ponds. High suspended solids ranked higher in jars (3) compared with Dubish ponds (8). The highest ranked hazards all lead to deformities which would persist through to later life stages. The top three ranked hazards also caused significant levels of mortality (greater than 40%). Water quality parameters score highly in part, because a high proportion of the population is affected (all the top hazards affected >40% of the populations and most affected greater than 60%). The most frequently occurring The EFSA Journal (2008) Annex I, 59-81

88 hazard was low water oxygen in Dubish ponds (low probability); all other highly ranked hazards occurred with very low or extremely low frequency. Table 8: Welfare risk ranking: eggs Jars water oxygen content too low water flow too low suspended solids too high water temperature too low / unionised ammonia content Dubish Pounds water temperature too low water oxygen content too low water flow too low water oxygen content too high / water temperature rapid change / water ph too high water flow too high Yolk sac fry Water quality parameters remained important for yolk sac fry in both tanks/troughs and Dubish ponds, notably low water oxygen and low water temperature. There were some interesting differences between the 2 systems. White spot disease was the highest ranked risk in Dubish ponds and only the 8 th ranked risk in tanks. Poor handling was important in jars but not Dubish ponds. The highest ranked hazards all resulted in deformities, have high severity scores and affect a high proportion of the population However, the probability of occurrence of hazards occurring was extremely or very low. Table 9: Welfare risk ranking: yolk sac fry Trough or Tank water oxygen content too low water flow too low suspended solids too high water oxygen content too high / handling not in acorrdance with best practice Dubish ponds White Spot Disease water oxygen content too low / water temperature too low unionised ammonia content water oxygen content too high / water temperature rapid change water temperature too low / unionised ammonia content The EFSA Journal (2008) Annex I, 60-81

89 Free living fry The top ranked hazards in all three systems were similar. Whilst water parameters remain important, shortage of natural food is the most important hazard for all systems. This hazard results in deformities. The hazard attains a high score because its severity is high, and it affects a high proportion of the population. The dependence of the life stage on natural food means that intervention to mitigate the impact is limited. Water quality parameters and temperature (too high or too low), white spot and Saprolegnia are important in all three systems. Inappropriate design of the pond was considered an important hazard for all three systems. Too high a temperature was the hazard with the highest probability of occurrence which had a low probability. Table 10: Welfare risk ranking: free living fry Dubish ponds Nursing ponds Fingerling ponds shortage of natural food long term water temperature too high / water oxygen content too low / water temperature too low pond size, morphology and substrate / water ph too low / water ph too high / White Spot Disease shortage of natural food long term water temperature too high / water oxygen content too low / water temperature too low pond size, morphology and substrate / White Spot Disease / Saprolegnia shortage of natural food long term water temperature too high / water oxygen content too low / water temperature too low pond size, morphology and substrate /White Spot Disease / Saprolegnia Nursed fry For both production systems, a lack of food supply continues as the most important hazard from the free living to the nursed fry stage. The hazards are very similar for both systems: low water oxygen, too low temperature and high unionised ammonia content. The main impact of the top ranked hazards remains deformities. The highest ranked hazards had high severity scores and affected a high proportion of the population, but occurred with very low or extremely low probability. Table 11: Welfare risk ranking: nursed fry/nursing Nursing Pond Fingerling Pond shortage of natural food long term water oxygen content too low /water temperature too low shortage of natural food long term water oxygen content too low / water temperature too low The EFSA Journal (2008) Annex I, 61-81

90 unionised amonia content water temperature too high water flow too low / water temperature rapid change / water ph too low / water ph too high / suspended solids too high unionised amonia content water temperature too high water flow too low / water temperature rapid change / water ph too low / water ph too high / suspended solids too high Fingerlings At this life stage there is only one production system. The top three hazards remain the same as the previous life stage. A long term shortage of food is the 4 th highest ranked hazards. At this life stage hazards result in reduced growth and poor condition (as well as mortality). The hazard which occurred with the highest probability was low oxygen (low probability). Predation also occurred with low frequency, and resulted in considerable mortality. Its severity at this life stage is low since mortality was the most common outcome, not injury. On some farms predation will occur with moderate or high frequency. Table 12: Welfare risk ranking: fingerling Fingerling Ponds water oxygen content too low water temperature too low unionised amonia content to high shortage of natural food long term water temperature too high / water temperature rapid change Over-wintering Over-wintering carp may be kept in over-wintering or grow-out ponds but the most important hazards are the same: low water oxygen, predators and low water flow (leading to hypoxia). Hypoxia results in stress and mortalities. Predation can lead to mortalities but from a welfare point of view, stress and physical damage to survivors can also occur. Too low temperature or rapid changes in temperature were highly ranked because they may lead to stress. There are clearly interactions between some hazards. Stress may result in an increased risk of disease as well as directly affecting the carp s welfare. Table 13: Welfare risk ranking: Over wintering Over wintering ponds Grow out ponds water oxygen content too low water oxygen content too low The EFSA Journal (2008) Annex I, 62-81

91 predators water flow too low water temperature rapid change / water temperature too low / unionised ammonia content water flow too low predators water temperature rapid change / water temperature too low / unionised ammonia content On-growers On-growers may be kept under intensive or extensive conditions. Interestingly, a very similar ranking of hazards are found in both systems: low water oxygen, rapid change in temperature, low water temperature and low ph. Rapid changes in temperature stress carp, the other hazards result in reduced growth and more chronic low level stress. Pollution is an important hazard in extensive but not intensive systems, whist lack of natural food occurs in intensive but not to the same extent in extensive systems. Predation was the 8 th highest ranked hazard. In some farms it is likely to be one of the most important welfare issues. At this, and later, life stage, predation is more likely to result in physical damage leading to a long duration of effect. Table 14: Welfare risk ranking: on growing Intensive on growing pond water oxygen content too low water temperature rapid change water flow too low / water ph too high unionised ammonia content h water ph too low Extensive on growing pond water temperature rapid change water oxygen content too low water flow too low / water ph too low / water ph too high pollution (sewage/industrial/agricultural run off) Marketable fish Marketable fish are only kept in storage ponds. The hazards are very similar to on-growers: low water oxygen, rapid change in temperature and low temperature. This is the only life stage where the top three ranked hazards all occur with low probability. Thus the highest ranked hazards collectively occur more frequently at this life stage than any other. Table 15: Welfare risk ranking: marketable fish Storage ponds water oxygen content too low water temperature rapid change / water temperature too low The EFSA Journal (2008) Annex I, 63-81

92 water flow too low / water ph too low water depth too shallow / unionised ammonia contenth Broodstock Broodstock fish are only kept in storage ponds. The hazards are very similar to on-growers and marketable fish: low water oxygen, rapid change in temperature and low temperature. The top ranked hazards all occurred with a very low probability. The top 3 ranked hazards all affected between 60-80% of the population; low water oxygen was highest ranked due to its higher severity score (4) compared with other hazards. Again, predation was the 8 th highest ranked hazard. In some farms it is likely to be one of the most important welfare issues. Table 16: Welfare risk ranking: broodstock Broodstock Ponds water oxygen content too low water temperature rapid change / water temperature too low / water ph too high water flow too low / water temperature too high Uncertainty All the highest ranking hazards had an uncertainty score of low or medium. Medium levels of uncertainty were for suspended solids (eggs, yolk sac fry) water ph (marketable, broodstock), dissolved oxygen (yolk sac fry), water flow (over-wintering, on-growers, marketable). Uncertainty was scored based on available information. For all hazards considerable variation will exist between farms, regions and over time. This has been captured to some extent by the ranges represented by each score; however, this has not been quantified (using confidence limits) in the final risk score. When assessing the risk scores, they should be viewed as the median value with a high standard deviation Mortality Low oxygen is the most important cause of mortality, having a high score (>3) in every life stage. Low water flow is an important cause of mortality in the later life stages. This is due to the associated reduction in available oxygen. Three hazards cause high levels of mortality (score >3) for yolk sac fry and on-growers. Of the selected diseases assessed, white spot was noted as an important cause of mortality for yolk sac and free-swimming fry. Table 17: Mortality scores >4 and 5 for the top 6 ranked hazards for each life stage. Hazard Life stage Handling Low O 2 White spot ph Low water Pollution Unionised ammonia The EFSA Journal (2008) Annex I, 64-81

93 Fertilised eggs/embryo Yolk sac fry 4d 5 5a Free swimming fry 5 5b Nursed fry 4 Fingerling 1 5 Over-wintering carp 5 flow 4 4 On-growers c Marketable fish 4 4 Broodstock 4 a Dubish ponds, b nursing ponds, c intensive on-growing ponds, d tank/trough 1 predation is also an important cause of mortality General discussion It is worth noting that the hazards were not distinguished by their duration of effect which generally were the same for all hazards within each life stage. The other main trend was that highly ranked risks generally affected a high proportion ( 60%) of the population and exerted severe effects (scores 3). However, the probability of occurrence was generally extremely low or very low. A few water quality parameters occurred consistently across life stages: high or low water temperature (or rapid temperature change), low water flow, low water oxygen, high or low ph. These hazards occur relatively infrequently (extremely or very low frequency), however, when they do occur the impact is severe and affects a high proportion of the population. The risk assessment cannot assess interactions between hazards. Environmental and in particular climatic conditions may simultaneously cause more than one hazard. It is possible that the resultant impact of one or more hazards, occurring at the same time, is synergistic. Oxygen paradoxically appears as an important welfare hazard in the risk assessment, although it is usually commonly accepted that carp are tolerant to low water oxygen concentration (as low as 0.9 mg/l section 5.1.4). However, welfare issues arise before lethal limits are reached. Also, severe oxygen shortage (e.g. collapse of algal blooms) was identified as major welfare issues. Apart from water quality issues, food shortage, disease and handling featured as highly ranked hazards. White spot was an important hazard for yolk sac fry in Dubish ponds but not other production systems. However, both white spot and Saprolengia were important at the next life stage (free living fry) in all 3 systems. Diseases did not rank highly for the older life stages. Handling only ranked in the top 6 hazards for yolk sac fry raised in tanks or troughs. Broodstock are handled for purposes of reproduction but the duration of the effect of handling is short-lived, resulting in a low score compared with other hazards. Long term food shortage was an issue at the fry and fingerling stages. The EFSA Journal (2008) Annex I, 65-81

94 Risk mitigation Monitoring water quality and the capacity to take remedial action would improve welfare in all life stages. In the early life stages, production in Dubish ponds may be less amenable to rapid and effective intervention compared with other production systems. The farmer s ability to mitigate environmental factors affecting many water quality and temperature hazards is limited in most carp production systems. The most important hazards occur relatively infrequently (very or extremely low frequency) and for short periods. This reduces the intervention opportunities for aquaculturists as by the time the hazard has been noted, the damage may have occurred. Reducing the impact of these hazards probably depends on developing systems and management strategies that are less susceptible to environmental and climatic changes. As an example, high levels of stocking will clearly exacerbate the impact of adverse climatic conditions causing low levels of dissolved oxygen or high levels of unionised ammonia. Of the hazards that can be described as management related only shortage of feed (during fry and fingerling stages) and handling, featured as highly ranked risks. Training and adoption of good codes of practice can reduce the impact of handling on the welfare of carp. Production systems which result, even relatively infrequently, in food shortages may be considered suboptimal from a welfare point of view. Most carp production relies on natural productivity for some of the life stages. It is therefore inevitable that potentially, more vulnerability to shortages of feed exist compared with other types of finfish production. This is especially true for the early life stages of fish. Commercially available diets are either expensive and/or unsuitable for extensive carp farming. Pond preparation and the creation of optimal conditions for the development of natural food items is therefore vital. The design and construction of carp farms (location, size of pond, etc.) and management regime (e.g. stocking rate) should always consider continuous adequate feed supply a priority. The EFSA Journal (2008) Annex I, 66-81

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105 The EFSA Journal (2008) Annex I, APPENDIX A. Risk assessment tables (link) APPENDIX B. Carp farming system European Food Safety Authority, 2008