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Aquaculture production continues to increase to satisfy global demand, and as such, issues relating to its environmental sustainability and the welfare of fish are becoming more prominent within society. Sterile triploid fish (possessing one additional chromosome set to the more natural diploid state) are in use in aquaculture and fisheries management to avoid the problems associated with unwanted early sexual maturation and genetic interactions between wild and cultured fish. Triploids are physiologically and behaviorally similar to diploids, although ploidy effects do exist. This review focuses on the welfare of triploid fish within aquaculture and fisheries management. The main conclusions are that triploids appear more susceptible to temperature stress, have a higher incidence of deformities, and are less aggressive than their diploid counterparts. However, considerable knowledge gaps exist in triploid physiology and performance; therefore, triploid requirements for water quality, nutritional requirements, stocking densities, and slaughter methods cannot be fully assessed. In addition, other than growth and survival, no information exists on the performance of triploids when released into natural environments, and this is of considerable concern, as triploids are commonly used in catch-and-release fisheries. These matters become more pressing with today's increased emphasis on animal welfare
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Published in Reviews in Fisheries Science (2012), Volume 20, Issue 4, Pages 192-211
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doi: 10.1080/10641262.2012.704598
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http://www.tandfonline.com/doi/abs/10.1080/10641262.2012.704598#.UyKrss7Z7DM
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Welfare considerations of triploid fish
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Thomas W. K. Fraser*1, Per Gunnar Fjelldal2, Tom Hansen2, Ian Mayer1
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1Department of Production Animal Clinical Sciences, Norwegian School of Veterinary
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Science, Postboks 8146 Dep, 0033 Oslo, Norway
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2Institute of Marine Research (IMR), Matre Research Station, 5984 Matredal, Norway
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*Author to whom correspondence should be addressed
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Address: Ullevålsveien 72, P.O. Box 8146 Dep., 0033 Oslo, Norway
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Tel: +47 (0) 22 96 48 63
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Fax: +47 (0) 22 59 70 81
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Email: tom.fraser@nvh.no
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Abstract
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Aquaculture production continues to increase to satisfy global demand, and as such, issues
21
relating to its environmental sustainability and the welfare of fish are becoming more
22
prominent within society. Sterile triploid fish (possessing one additional chromosome set to
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the more natural diploid state) are in use in aquaculture and fisheries management to avoid
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the problems associated with unwanted early sexual maturation and genetic interactions
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between wild and cultured fish. Triploids are physiologically and behaviourally similar to
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diploids, although ploidy effects do exist.
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This review focuses on the welfare of triploid fish within aquaculture and fisheries
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management. Our main conclusions are that triploids appear more susceptible to temperature
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stress, have a higher incidence of deformities, and are less aggressive than their diploid
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counterparts. However, considerable knowledge gaps exist in triploid physiology and
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performance, therefore triploid requirements for water quality, nutritional requirements,
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stocking densities, and slaughter methods cannot be fully assessed. In addition, other than
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growth and survival, no information exists on the performance of triploids when released into
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natural environments and this is of considerable concern, as triploids are commonly used in
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catch-and-release fisheries. These matters become more pressing with todays increased
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emphasis on animal welfare.
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Keywords: Ploidy, Diploid, Aquaculture, Stress, Cell size
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Introduction
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Aquaculture is the world’s fastest growing sector of animal production. Global fish
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production has been increasing at an annual rate of 8.7 % since 1970 (FAO, 2006) and
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currently accounts for over 47 % of the world’s total fish supply. Today, early un-wanted
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sexual (“precocious”) maturation is a major challenge in fish farming, particularly in
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salmonids, but also in other fishes including, sea basses, flatfishes, cod fishes, tilapias, sea
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breams, and perches (review, Taranger et al., 2010). Recently, losses due to sexual maturation
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in Atlantic salmon (Salmo salar) were estimated to account for an estimated 4 - 9 % of gross
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revenue in New Brunswick, Canada (based on a median level of sexual maturation of 6.6 %:
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McClure et al., 2007). In addition, genetic interactions between wild and escaped farmed fish
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are an environmental concern (McGinnity et al., 2003) calling into question the impact of
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aquaculture (including invertebrates; Piferrer et al., 2009) on environmental sustainability.
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Both of the aforementioned problems could be solved by the use of sterile fish.
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Triploids are individuals whose cells possess three complete sets of chromosomes, whereas
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diploids have two complete chromosome sets. While diploidy is the more natural state in all
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vertebrates, including teleosts, polyploidy, the state where an individual possess one or more
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additional chromosome set(s), occurs naturally (Thorgaard and Gall 1979; Purdom, 1984) and
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can be induced artificially in fish (review, Piferrer et al., 2009). Artificial triploids, produced
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by preventing the extrusion of the second polar body during the second meiotic division, are
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sterile (Benfey et al., 1989).
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Initial interest in triploids for use in aquaculture began in the mid 1970’s; however,
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production issues offset the advantages gained by sterility. Most significantly, triploid fish
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were reported to be more sensitive to production stressors when compared to diploid
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counterparts (Jungalwalla, 1991; Ojolick et al., 1995). This led to the abandonment of
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triploids in favour of more expensive and less effective methods to control early sexual
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maturation (e.g. photoperiod manipulation). However, the current concerns over the
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sustainability of the aquaculture industry, coupled with an increased understanding of triploid
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physiology and rearing requirements, have led to a renewed interest in the triploid concept.
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Today, the key triploid species for use in both aquaculture and/or fisheries management
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include salmonids, mainly rainbow trout (Oncorhynchus mykiss), brown trout (Salmo trutta)
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and Atlantic salmon, ayu (Plecoglossus altivelis), loach (Misgurnus anguillicaudatus), and
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grass carp (Ctenopharyngodon idella) (Powell et al., 2009; Beaumont et al., 2010).
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As a consequence of increased aquaculture production and use of fish models in research, fish
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welfare has become an increasingly prominent issue with policy makers, scientists, and
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consumers (Huntingford et al., 2006; Johansen et al., 2006). Whereas previously good welfare
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practices were sought in order to attain optimal growth, survival, and fecundity, today fish
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welfare is increasingly focusing on not just performance related characteristics, but also
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quality of life characteristics.
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Definitions of animal welfare are typically function-based, nature-based, or feelings-based
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(Huntingford et al., 2006). Briefly, these definitions encompass whether the animal 1) can
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adapt to its environment with all its biological systems working correctly, 2) can lead a
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natural life, expressing the same behaviour as found within the wild and, 3) is free from
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negative experiences such as pain, fear, and hunger and has access to positive experiences
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such as social companionship (Huntingford and Kadri, 2008). As there is considerable debate
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as to whether fish experience similar emotional states as humans (Rose, 2007; Sneddon,
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2009), physiology and behaviour (essentially points 1 and 2) are the most reliable indicators
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of fish welfare.
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Recent reviews have not only highlighted the species-specific differences in fish welfare
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requirements, but also the differences due to within species genomic variation (Chandroo et
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al., 2004). Previously, it had been suggested that triploids could be considered a separate
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species to diploids (Benfey, 2001) based on the physiological differences between triploids
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and diploids (reviews, Benfey, 1999; Piferrer et al., 2009), adding emphasis to the need to
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evaluate triploid fishes separately to their diploid counterparts.
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In view of the growing emphasis on improved fish welfare, this review aims to clarify
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whether welfare is likely to differ significantly between diploid and triploid fish based on
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function- and nature- based definitions. Where information is available, this review will cover
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those areas regarded as key to fish welfare from a biological perspective (Table 1), in
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aquaculture and fisheries management. To keep the review focused on the issue of triploid
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welfare, detailed information on the indicators of fish welfare (e.g. Håstein et al., 2005;
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Huntingford et al., 2006; Ashley, 2007; Cooke and Sneddon, 2007; Braithwaite and Salvanes,
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2010) and on the wider ethical issues surrounding the human use of fish (including GM fish:
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Myhr and Dalmo, 2005), fish liberation, and fish rights (Arlinghaus and Schwab, 2011;
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Arlinghaus et al., 2012), can be found elsewhere. In addition, references to non-artificial
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triploid fish will in the most part be avoided, as natural populations are not sterile (e.g.
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Lamatsch et al., 2010) and this may significantly influence their physiology. Initially, we
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provide a brief introduction to triploid induction, sterility, cell size, and heterozygosity,
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followed by the main discussion on triploid welfare in aquaculture and fisheries management.
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Artificial triploid induction and family effects
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The most common triploid induction methods in fish include temperature shock (heat and
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cold) and pressure shock, and these include a number of variables such as timing (dependant
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on temperature), intensity, and duration of the shock (review, Piferrer et al., 2009). The
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optimum methods, based on survival and success rate, would appear to differ between species
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and strain; therefore each species must be evaluated separately (Solar and Donaldson, 1985;
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Felip et al., 1997; Peruzzi et al., 2007). This is particularly important from an animal welfare
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perspective as unacceptably high mortality and deformity rates are caused by inefficient
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triploid induction procedures (e.g. Peruzzi and Chatain, 2000). In addition, there is a positive
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correlation between egg quality and triploid induction success (Aldridge et al., 1990; Palti et
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al., 1997).
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Family, strain, and/or induction method effects have been observed in triploid, induction
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success (Johnson et al., 2004), survival (Withler et al., 1995; Johnson et al., 2004), growth
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(Withler et al., 1995, 1998; Bonnet et al., 1999; Friars et al., 2001; Johnson et al., 2004;
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Shrimpton et al., 2007; Trippel et al., 2008; Chiasson et al., 2009; Sacobie et al., 2012),
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smolting (Withler et al., 1995; Shrimpton et al., in press), and immune response (Johnson et
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al., 2004). In addition, family × ploidy interactions have been observed in some studies
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(Withler et al., 1995, 1998; Bonnet et al., 1999; Friars et al., 2001; Trippel et al., 2008) which
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suggests families that perform best as diploids are not necessarily the best performers as
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triploids. However, Blanc et al. (2005) suggest that the reported ploidy effects may not be true
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ploidy effects, more a reflection of the variation in the maternal influence on performance
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traits due to the additional genetic material provided by the dam (when triploids are produced
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by prevention of the removal of the second polar body). Therefore, in selective breeding,
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more importance should be given to maternal selection than paternal selection. However, in
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all the aforementioned studies on ploidy and family effects, triploids have been compared to
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diploids in one environment (i.e. one temperature, a diet designed for diploids) considered
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within the optimum range for diploids. As we discuss below, triploids would appear to have
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at the very least different dietary requirements and temperature optima to diploids, and, as
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such, the family and ploidy effects should be taken with caution as they are likely biased
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towards diploid performance.
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Triploid sterility
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Artificial triploid induction leads to significant differences in the degree of gonadal
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development between the sexes, however, both remain sterile, as they are incapable of
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producing viable offspring (Peruzzi et al., 2009). For instance, females display severely
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underdeveloped ovaries and show no physiological or morphological signs of maturation
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(Benfey et al., 1989). In females, triploidy interferes with the normal pairing of homologous
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chromosomes during the initial phase of meiosis (Krisfalusi and Cloud, 1999), inhibiting
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further gamete development due to the lack of the hormone production in the theca and
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granulose layers of the follicle (Schafhauser-Smith and Benfey, 2003). In contrast, in males,
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triploidy blocks the late phases of meiosis (Krisfalusi and Cloud, 1999), allowing for full
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gonadal development due to the production of functional steroidogenic cells (Benfey et al.,
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1989). Therefore, in commercial species where early precocious maturation is an economic
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issue (i.e. rainbow trout) all triploid female stocks are used. However, the progeny of
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produced triploid males are aneuploid and do not survive beyond the embryonic or larval
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stages (Perruzi et al., 2009; Feindel et al., 2010). Therefore, although triploid males may
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participate in spawning events (Perruzi et al., 2009; Feindel et al., 2010) with diploids, it is
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unlikely that genetic introgression will occur with wild populations.
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Cell size
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To accommodate the additional chromosome set, triploid nuclear and cellular volumes are
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higher than in diploids, although the same nuclear to cytoplasmic ratio is maintained (Small
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and Benfey, 1987; Flajšhans et al., 2011). Therefore, as triploid organs are generally the same
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size as diploid counterparts, they are made up of fewer cells (Swarup, 1959; Aliah et al.,
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1990). However, this has not been certified in all cell types and likely does not apply to cells
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where the nucleus only occupies a small portion of the total cell volume (e.g. muscle cells
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were found to be only 30 % larger in triploids, Johnston et al., 1999). It remains unknown as
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to whether the increase in cell size lengthens signalling pathways or impairs transport
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processes across membranes (review Maxime, 2008). In addition, no information exists on
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the exact homeostatic mechanism(s) responsible for the observed cell number reduction in
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triploids.
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Heterozygosity and gene expression
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Triploid fish are generally more heterozygous than their diploid counterparts (Allendorf and
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Leary, 1984; Leary et al., 1985). Under optimum diploid conditions, triploids display similar
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gene expression patterns to diploids due to modulated gene expression (Johnson et al., 2007;
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Shrimpton et al., 2007; Garner et al., 2008; Ching et al., 2010). However, the mechanism by
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which the specific contribution of each genome is regulated in triploids has not yet been
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determined (Pala et al., 2008) and may be affected by stress (Ching et al., 2010).
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Welfare considerations of triploid fish in aquaculture and fisheries management
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The welfare of farmed animals is a central requirement of animal rearing systems, and
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currently the EU Council Directive 98/58/EC provides minimum standards for the protection
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of farmed animals, including that of fish. Within aquaculture, fish welfare is composed of
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several key topics that are affected on a species-specific basis (Huntingford et al., 2006).
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Welfare issues also exist for the release of reared fish into the environment (Table 2). Below
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we summarise the literature available on accepted biological and behavioural indicators of
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fish welfare (Table 1), and provide evidence that the prefered conditions under which diploids
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are kept are not necessarily the same for their triploid counterparts, especially with regard to
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water temperature. We also demonstrate that although triploid release programs are
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widespread, literature on the post release performance of triploids is minimal, with many of
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the acknowledged welfare indicators in released fish unreported for triploids.
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Survival
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The current literature would suggest triploid survival is comparable to diploid survival from
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post larval stages onwards. Although in the various development periods up to the larval
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stages triploids may display higher mortalities than diploids, the levels are within the accepted
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industrial limits if the induction procedure is optimised (review, Piferrer et al., 2009).
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Examples of similar post larval survival rates between triploids and diploids exist in a number
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of species including Atlantic salmon (Oppedal et al., 2003), rainbow trout (Bonnet et al.,
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1999), and sea bass (Dicentrarchus labrax) (Felip et al., 2001). As in diploids, there exists
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variability in triploid survival between families (Johnson et al., 2004). However, families that
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perform well as diploids do not necessarily perform well as triploids (Taylor et al., 2011). In
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addition, Taylor et al. (2011) observed that egg quality had a more significant effect on
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survival than ploidy state in Atlantic salmon, with triploid mortalities increasing significantly
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compared to diploids when both were reared from low quality eggs (those eggs beginning to
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enter the over-ripening period). Therefore it would seem essential to use high quality eggs for
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triploid production.
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In the instances of decreased juvenile and adult triploid survival, compared to diploid
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counterparts, the cause of death is often related to periods of high water temperatures and
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hypoxia (Myers and Hershberger, 1991; Blanc et al., 1992; Ojolick et al., 1995). Notably, the
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only controlled study to examine the effects of both chronic high water temperature and
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hypoxia in triploid fish reported significantly increased mortalities in triploid Atlantic salmon
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when exposed to combinations of high temperatures (19 °C) and hypoxia (70 %) in seawater
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(Hansen et al, in prep). However, no ploidy effect on mortality was observed in fish exposed
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to only high temperature as seen in other studies (Benfey et al., 1997; Galbreath et al., 2006).
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One area where triploids consistently outperform diploids in survival rates is during the
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stressful period of sexual maturation (Inada and Taniguchi, 1991; Yamamoto and Iida, 1995a;
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Gillet et al., 2001; Cal et al., 2006). The general consensus is that the increases in plasma
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steroid levels (i.e. testosterone and 11-ketotestosterone) that occur concurrent with sexual
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maturation results in progressive immunosuppression and altered health status in the fish
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(Slater and Schreck, 1997; Harris and Bird, 2000). Therefore, as triploid females do not
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undergo maturation (Benfey et al., 1989) their immune system is not compromised by the
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prolonged elevation of plasma sex steroids (Yamamoto and Iida, 1995a).
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For stocking purposes, the survival of triploid fish compared to diploids has been assessed in
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salmonid species, with evidence suggesting triploids perform poorly in more variable
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environments. For example, recapture rates of triploid rainbow trout were lower compared to
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diploids in three South Dakota ponds (Simon et al., 1993), in high mountain lakes (Kozfkay et
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al., 2006; Koenig et al., 2011), Alaskan lakes (Havens and Sonnichsen, 1993; Rutz and Baer,
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1996), and Idaho lakes (Koenig and Meyer, 2011). However, triploid performance has been
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reported to be equal to that of diploids in eighteen Idaho streams (Dillon et al., 2000), in a
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spring-fed lake (Wagner et al., 2006), and in an Idaho river (no diploid controls, results
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compared to previous findings: High and Meyer, 2009) or greater in two Idaho reservoirs
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(Teuscher et al., 2003). Where triploid mortalities exceed that of diploids, it is suggested to be
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related to habitat quality, with triploid survival impaired in lower quality environments (i.e.
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larger temperature fluctuations and periods of low oxygen levels: Simon et al., 1993; Koenig
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and Meyer, 2011), however, no study has specifically addressed this issue.
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After marine release, triploid Atlantic salmon return rates were lower than diploids in both
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sexes (Cotter et al., 2000; Wilkins et al., 2001). It is unclear whether the later findings are
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caused by differences in survival or impaired migratory behaviour. Although the reduced
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return rates of triploid females is most likely explained by their low levels of reproductive
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hormones (Inada and Taniguchi, 1991; Warrillow et al., 1997; Cotter et al., 2000), this does
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not apply to triploid males that do mature (Benfey et al., 1989). Interestingly, we recently
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found triploid pre-smolt Atlantic salmon to have a smaller (approx. 9 %) olfactory bulb than
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diploid counterparts (Fraser et al., submitted); olfactory senses are important for the homing
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behaviour in salmonids (Nevitt et al., 1994).
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Growth and nutrition
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Using growth as an indicator of stress in triploids is compromised by a lack of consistent data
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on triploid growth performance. While many studies have compared growth performance
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between diploid and triploid conspecifics, results have been inconsistent; with improved,
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equal, and poorer growth rates being reported between the ploidy states (review Piferrer et al.,
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2009). Reasons for the inconsistent growth responses for triploids include stage of
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development, the impact of communal rearing with diploids, sex ratios, genetic variation, and
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no systematic study of the optimum conditions for triploid growth (i.e. optimum conditions
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are assumed to be equal to diploids). However, there is a general trend for triploids to show
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reduced growth in the early life stages compared to diploids, but similar growth in the later
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life stages (after first feeding).
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Although triploids are predominantly used in global rainbow trout production, there is
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surprising little information available on triploid dietary requirements. Reports suggested that
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although the ploidy state does not affect food utilization (Oliva-Teles and Kaushik, 1987,
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1990a, 1990b), the ability to oxidize glucose and amino acids (Fauconneau et al., 1986,
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1989), energy balance (Wiley and Wike, 1986), or protein efficiency ratios (Pechsiri and
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Yakupitiyage, 2005), ploidy effects have been reported in amino acid levels (Buchtová et al.,
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2004, 2005a, 2005b), proximate composition (Segato et al., 2006; Burke et al., 2010), the
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response to restricted feeding (Byamungu et al., 2001), fat deposition in the viscera of
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females (Lincoln and Scott, 1984; Hussain et al., 1995; Koedprang and Na-Nakorn, 2000;
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Peruzzi et al., 2004), condition factor (O’Flynn et al., 1997; Oppedal et al., 2003; Blanc et al.,
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2005), and, in contrast to above, nitrogen and energy efficiency ratios (Burke et al., 2010).
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To date, triploids have been fed on diets formulated for diploid fish on the presumption that
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triploids have the same dietary requirements. However, in a recent study it was found that
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triploids required elevated dietary phosphorus compared to diploids, based on the
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development of skeletal deformities (Fjelldal et al., 2011).
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Growth performance data on triploids in the wild is generally lacking, however, the general
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trend is of poorer growth in triploids in comparison to diploids. Simon et al. (1993) reported
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poorer growth of triploid rainbow trout in comparison to diploids in three South Dakota ponds
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possibly due to the summer conditions that resulted in high water temperatures and hypoxic
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conditions (no values given for either). In addition, triploid rainbow trout (Havens and
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Sonnichsen, 1993) and chinook salmon (Rutz and Baer, 1996) were significantly smaller than
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diploids in Alaskan lakes. Tuescher et al. (2003) reported differences in ontogenetic growth
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between diploids and triploids, with equal performance in the first year before diploids
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growing heavier than triploids in the second and third year. However, no ploidy effects were
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reported in rainbow trout stocked in Idaho alpine lakes (Koenig et al., 2011) or Idaho lakes
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and reservoirs (Koenig and Mayer, 2011).
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Acute stress response
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The literature would suggest that triploid salmonids perform similarly to diploids under
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stressful production procedures. For example, the primary (i.e. cortisol) and secondary stress
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responses (i.e. osmoregulation, plasma glucose, haemological) of triploid salmonids and
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sturgeon (Acipenser brevirostrum) are similar to diploids after netting and confinement
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(Biron and Benfey, 1994; Benfey and Biron, 2000; Sadler et al., 2000a, 2000b), or chasing
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(Beyea et al., 2005; Kobayashi et al., 2009).
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Cortisol is generally regarded as the most robust and reliable indicator of stress in fish and is
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linked to many of the adverse outcomes to chronic stressors (Pottinger, 2008). Although
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several studies have reported plasma cortisol levels in triploids (Biron and Benfey, 1994;
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Benfey and Biron, 2000; Sadler et al., 2000a, 2000b; Beyea et al., 2005; Peruzzi et al., 2005;
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Leggatt et al., 2006; Garner et al., 2008) no information exists on triploid cortisol receptor
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abundance or affinity, or molecular biology (i.e. mRNA). Without this information, it is
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difficult to fully assess the triploid stress response and welfare state.
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Acute transport stress
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Studies on the effects of transport stress on triploid fish would suggest they respond similarly
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to diploids. For example, after an 8 hr transport period, there were no discernible ploidy
2
differences in the endocrine (plasma cortisol and glucose) and cellular (hepatic GSH and heat
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shock protein (HSP) 70) stress response of juvenile rainbow trout (Leggatt et al., 2006).
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Similarly, no ploidy differences were observed in mortality rates in three strains of rainbow
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trout 96 hrs after a 4 hr transport period at high stocking densities (100 g l-1) followed by
6
stocking in various different scenarios of pH (max 9.34) and high water temperature (max 21
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˚C) (Wagner et al., 2006).
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Immune response and disease
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In contrast to anecdotal reports, laboratory studies would suggest the fish immune system is
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not impaired in triploids. For instance, Ojolick et al. (1995) reported increased disease
12
susceptibility in triploid rainbow trout compared to diploid counterparts, whilst Ozerov et al.
13
(2010) reported increased Gyrodactylus infection in triploid Atlantic salmon. In contrast,
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although triploid immune cells are typically larger and fewer in number than in diploids (as
15
also seen with erythrocytes), in vitro studies provide evidence of similar respiratory burst
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activity and phagocytosis per microlitre of blood in triploid and diploid neutrophils (Budiño
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et al., 2006). Complement and neutrophil activity were also similar in triploid and diploid
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rainbow trout (Yamamoto and Iida 1995b). In addition, diploids and triploids typically have
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similar cell differentiation counts in salmonids (Benfey and Biron, 2000; Dorafsen et al.,
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2008), turbot (Psetta maxima) (Budiño et al., 2006), and tench (Tinca tinca) (Svobodová et
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al., 2001). In contrast, Fraser et al. (2012) found ploidy related differences in the proportion
22
of neutrophils and B-cells in the peripheral blood and head kidney of Atlantic salmon post
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smolts. B-cells were more affected by ploidy than neutrophils, with triploids having lower
24
values than diploids. However, the majority of in vivo challenge studies against a range of
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common diseases, such as vibrio (Inada et al., 1990; Kusuda et al., 1991; Ching et al., 2010),
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Aeromonas salmonicida (Yamamoto and Iida, 1995c), A. hydrophila (Na-Nakorn and
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Lakhaanantakun, 1993) Renibacterium salmoninarum (Bruno and Johnstone, 1990),
28
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infectious hematopoietic necrosis virus (Parsons et al., 1986), viral haemorrhagic septicaemia
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virus (Dorson et al., 1991), infectious pancreatic necrosis virus (Dorson et al., 1991), and
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lipopolysaccharide (Langston et al., 2001) have seen little or no effect on the results due to
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ploidy, although exceptions do exist (Yamamoto and Iida, 1994; Jhingan et al., 2003).
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However, in studies on cell counts, triploid fish would appear to demonstrate a higher
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percentage of deformed or irregular immune cells (Wlasow et al., 2004; Wlasow and Fopp-
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Bayat, 2011), similar to reports of higher percentage of irregular red blood cells in triploids
7
compared to diploids (see below).
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9
In those studies reporting increased disease susceptibility in triploids, the authors typically
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report the fish to be exposed to high water temperatures (Myers and Hershberger, 1991;
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Ojolick et al., 1995; Cotter et al., 2002; Ching et al., 2010). Therefore, it could be that
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triploids have a sub-par immune system that is more critically affected by temperature stress,
13
which is not evident in those trials only investigating immune response or infection rates. A
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possible explanation for the reduced immunocompetence of triploids could be attributed to
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stress altering the mechanism that controls the expression of the extra genetic material within
16
triploids, as recently suggested by Ching et al. (2010). In the latter study, the expression of
17
constitutively expressed genes, immunoglobulin (Ig) M, major histocompatibility complex II
18
and β-actin, was altered by ploidy manipulation after a live V. anguillarum exposure in
19
chinook salmon (Oncorhynchus tshawytscha). Or alternatively, triploids have a decreased
20
capacity to deal with stress due to decreased erythrocyte numbers for immunosurveillance,
21
and decrease cross-talk between cells and the extra cellular milieu, which negatively
22
influences cell communication, signal transduction, and other processes, such as cell
23
movements or a rise in oxygen consumption associated with immunocyte activation (Ballarin
24
et al., 2004). Interestingly, Cantas et al. (2011), suggested juvenile triploid Atlantic salmon
25
may be more prone to opportunistic pathogens compared to diploids, due to increased levels
26
of bacteria found within the triploid gut (including Vibrio spp.), and this may further increase
27
the susceptibility of triploids to pathogens when stressed.
28
15
1
Triploid fish have demonstrated a similar response to vaccination as diploids. For instance, no
2
ploidy effect was reported on agglulating antibody titres, complement activity or phagocytic
3
activity in ayu vaccinated with formalin killed V. anguillarum (Kusuda et al., 1991). In
4
addition, no ploidy related differences were seen in rainbow trout vaccinated against vibrio
5
and subsequently subjected to a challenge trial with V. ordalii (Yamamoto and Iida, 1995c) or
6
in the antibody response to Listonella anguillarum in chinook salmon (Johnson et al., 2004).
7
However, there was a significant ploidy × vaccination interaction in neutrophil and B-cell
8
proportions in underyearling Atlantic salmon post smolts, but no ploidy × vaccination
9
interaction was observed in sibling yearlings (Fraser et al., 2012).
10
11
Several toxicological experiments would suggest triploid are more resistant to disease than
12
diploids. For instance, triploid rainbow trout exposed to three carcinogens (DMBA, MNNG,
13
and aflatoxin B1) display a lower incidence of tumours in the swimbladder, stomach, and
14
kidney (Thorgaard et al., 1999). Similarly, while no differences in growth were observed
15
between diploid and triploid rainbow trout exposed to aflatoxin B1, triploids showed reduced
16
levels and slower progression of neoplastic lesions compared to diploids (Arana et al., 2002).
17
These results are possibly due to additional copies of tumour suppression genes in triploids.
18
Thus, the limited evidence available suggests that triploid fish may show a greater tolerance
19
to anthropogenic pollutants compared to diploid conspecifics.
20
21
22
Behaviour
23
There is sufficient literature to suggest triploids are less aggressive than their diploid
24
counterparts during the juvenile stage (Table 3). A behavioural difference may explain some
25
of the reduced growth rates (Thorgaard et al., 1982; Galbreath et al., 1994) and increased fin
26
erosion when triploids are reared together with diploids (O’Flynn et al., 1997; Bonnet et al.,
27
1999; Blanc et al., 2005). A reason for the reduction in triploid aggression could be due to
28
16
reduced sensory perception caused by reduced cell numbers in the sensory organs (Swarup,
1
1959; Aliah et al., 1990). However, although triploids appear less aggressive when reared on
2
their own, this result is not always repeated when reared communally with diploids (Wagner
3
et al., 2006; Garner et al., 2008). In addition, to date all studies on triploid salmonid behaviour
4
have been on juvenile fish. Therefore, no evidence exists for behavioural differences beyond
5
the typically more territorially motivated parr stage.
6
7
The current literature suggests that triploids are inferior to diploids in foraging performance
8
and in some cases food competition. For instance, when compared to diploid conspecifics,
9
juvenile hybrid triploid saugeyes (Stizostedion vitreum x S. canadensis) displayed altered prey
10
selection (59 % and 39 % of available fathead minnows (Pimephales promelas), respectively)
11
while consuming more daphnia (Daphnia pulex), had more attempted attacks (20 versus 29
12
per predator per feeding session, respectively) with an increased percentage of failed attempts
13
(48 % versus 62 %, respectively), and increased handling time of a single large minnow
14
(Czesny et al., 2002). Therefore, it was concluded that juvenile triploid saugeyes were less
15
efficient at foraging compared to diploids, potentially reducing triploid growth rate,
16
increasing triploid predation risk, and decreasing triploid survival. In terms of food
17
competition the evidence is mixed, but several studies have reported poorer competitive
18
ability in triploids when compared to diploids within the culture environment (Table 3). These
19
results are suggestive of triploids having a lower lifetime fitness compared to their diploid
20
counterparts.
21
22
There is strong evidence to suggest triploidy has sex specific differences on reproductive
23
behaviour. Several investigators have demonstrated that female triploid fish rarely participate
24
in spawning migrations (Inada and Taniguchi, 1991; Warrillow et al., 1997; Cotter et al.,
25
2000) whereas not only do males participate in spawning migrations, they are also capable of
26
courtship behaviour and inducing spawning in female diploids (Inada and Taniguchi, 1991;
27
Kitamura et al., 1991; Iguchi and Ito, 1994; Brämick et al., 1995; Peruzzi et al., 2009). These
28
17
pronounced gender differences in reproductive behaviour are most likely a consequence of
1
the impaired gonadal development and reduced plasma steroid levels displayed by triploid
2
females in contrast to triploid males which display more advanced gonadal development and
3
normal levels of plasma steroids required for triggering male sexual behaviour (Benfey et al.,
4
1989). However, artificial fertilisation trials crossing triploid sperm with diploid eggs of
5
Atlantic cod (Gadus morhua) have produced progeny that are aneuploid and die at the
6
embryonic or larval stages (Peruzzi et al., 2009). Therefore, there is the possibility of triploid
7
fish participating in wild spawning events and producing progeny displaying poor survival
8
(reduced life-time fitness), and this could be considered a welfare issue.
9
10
The ability of fish to learn is an important aspect for the welfare of released fish. The learning
11
processes may also be interfered with by stress (Olla and Davis, 1989). The sole study on the
12
learning ability of triploid fish observed no ploidy effect on the ability of brook trout to learn
13
to avoid an electrical shock using a Y-maze test (Deeley and Benfey, 1995). In addition, we
14
found no effect of ploidy on brain size (indirect measure of cognitive ability) in pre-smolt
15
Atlantic salmon (Fraser et al., submitted).
16
17
Production disorders
18
Skeletal deformities
19
At present, the high prevalence of deformities is the major constraint on the expansion of
20
triploid aquaculture (Taranger et al., 2010). Triploids demonstrate the same production
21
deformities as seen in diploids, only a higher incidence is typically reported in triploids
22
(Table 4).
23
24
Several studies have reported a higher occurrence of lower jaw deformities (LJD) in triploid
25
salmonids compared to diploids (e.g. Sutterlin et al., 1987; Benfey, 2001; Sadler et al., 2001).
26
Lijalad and Powell (2009) studied the physiological effect of LJD in all female diploid and
27
triploid Atlantic salmon, and found no effect of either ploidy or LJD on critical swimming
28
18
speed, but that triploids with LJD were not capable of attaining the same critical swimming
1
speed after a 45 min recovery. Phosphorous deficiency during freshwater rearing has been
2
shown to induce LJD in both diploid and triploid Atlantic salmon, although the effect was
3
most pronounced in triploids (Fjelldal et al., 2011). Roberts et al. (2001) studied LJD in
4
newly seawater transferred Atlantic salmon smolts in Chile, and suggested that rapid jaw
5
movement caused by increased respiration rate due to high feeding levels and low dissolved
6
oxygen levels at high water temperature can cause LJD if the bone of the lower jaw is not
7
properly mineralized. Hence, the higher demand for dietary phosphorous to achieve proper
8
bone mineralization (Fjelldal et al., 2011) in combination with a reduced oxygen carrying
9
capacity (Bernier et al., 2004) in triploids, when compared to diploids, may make them more
10
prone to develop LJD.
11
12
There are also reports of higher occurrences of vertebral deformities in triploids than diploids
13
(Madsen et al., 2000; Fjelldal and Hansen, 2010; Grimmett et al., 2011), with the predominate
14
location being beneath the dorsal fin for both Atlantic salmon (Fjelldal and Hansen, 2010)
15
and grass carp (Grimmett et al., 2011). Previously vertebral deformities have been shown to
16
impede swimming performance and impose a significant metabolic cost in both triploid and
17
diploid Atlantic salmon (Powell et al., 2009), both important indicators of fish welfare. In
18
cultured diploid Atlantic salmon, the development of vertebral deformities has been linked to
19
unfavourable conditions during egg incubation (Wargelius et al., 2005), vaccination (Berg et
20
al., 2006), under-yearling smolt production (Fjelldal et al., 2006), dietary phosphorous
21
(Baeverfjord et al., 1998; Fjelldal et al., 2009), and elevated water temperature (Grini et al.,
22
2011). In triploids, vertebral deformities were found to be most prevalent in the fastest
23
growing triploid families of Atlantic salmon, suggesting a growth or genetic component
24
(Leclercq et al., 2011). In addition, dietary phosphorus requirements are affected by triploidy.
25
Fjelldal et al. (2011) fed diploid and triploid Atlantic salmon siblings diets with a phosphorus
26
level that were deficient, within, or higher than the estimated requirement range of diploids
27
from first feeding to the smolt stage, and found a higher occurrence of vertebral deformities
28
19
for the low and medium diet, and a low and equal deformity incidence in diploids and
1
triploids for the high phosphorous diet. Interestingly, in the latter study, the vertebral bone
2
mineral content at the smolt stage was equal for diploids and triploids for the low and high
3
phosphorus diets, and lower in triploids compared to diploids for the diet with a phosphorus
4
level within the estimated requirement range of diploids. This may indicate that the dietary
5
requirement for phosphorus is effected by ploidy in Atlantic salmon. In contrast, a similar
6
study by Burke et al. (2010), also in Atlantic salmon, found no difference in bone mineral
7
content between diploids and triploids fed various dietary levels of phosphorus. However,
8
Fjelldal et al. (2011) fed salmon from first feeding, whereas Burke et al. (2010) began the
9
experiment with 45 g fish. Hence, it may be that triploids have a higher demand for
10
phosphorous only during the early juvenile stages, at a smaller size than Burke et al. (2010)
11
tested.
12
13
Ocular cataracts
14
Ocular cataract prevalence is consistently found to be higher in triploid than diploid Atlantic
15
salmon, the only triploid fish species to be assessed for this deformity (Table 4). Leclercq et
16
al. (2011) observed increased cataract prevalence and severity in two full-sib families of out-
17
of-season triploid smolts compared to diploid counterparts, with macroscopic cataracts
18
present from six months post-seawater transfer. In contrast to diploids, triploid cataracts were
19
consistent with defective ocular osmoregulation due to the type and location of the lesion.
20
Wall and Richards (1992) also reported more severe ocular cataracts in triploid Atlantic
21
salmon compared to diploid counterparts. Cataract formation is linked to a variety of
22
causative factors; however, Leclercq et al. (2011) suggested an increase in water temperature
23
and rapid growth rates (during the summer months), and/or nutritional deficiencies (i.e.
24
Histidine) were the most likely cause of cataract formation in their study.
25
26
Fin erosion
27
20
Although few studies have investigated fin erosion in triploids, evidence would suggest fin
1
erosion is either equal or reduced in triploids reared separately from diploids. For instance,
2
when reared separately from diploids, triploids displayed similar caudal and dorsal fin
3
damage in Atlantic salmon parr (Carter et al., 1994), whereas in three strains of rainbow trout,
4
triploids were found to have longer dorsal, caudal, anal, pelvic, and pectoral fins than
5
diploids, although exceptions were noted between strains for the dorsal and left pelvic fins
6
(Wagner et al., 2006). However, when mixed with diploids, triploids had more severe damage
7
to the dorsal fin than diploids in Atlantic salmon (Carter et al., 1994) that could be linked to
8
suggestions that diploids are more aggressive than triploids. Of note, triploid rainbow trout
9
have been reported to show greater fin regeneration rates than diploids (Alonso et al., 2000), a
10
trait that may be advantageous from a welfare point of view.
11
12
Vaccination
13
Triploids demonstrate some of the same side effects to commercial vaccination seen in
14
diploid Atlantic salmon. For instance, we observed a similar percentage reduction in triploid
15
growth after vaccination as seen in diploids after the first summer in seawater (Fraser et al.,
16
unpublished data). In addition, triploids demonstrate the vaccine-induced abdominal lesions
17
previously reported in diploids (Midtlyng et al., 1996), however the severity of the lesions
18
would appear to be increased in triploid under-yearlings compared to diploid counterparts,
19
however no ploidy effect was observed in yearlings (Fraser et al., unpublished data).
20
21
Environmental preferences
22
Temperature
23
Triploids have been reported to perform poorly in comparison to diploids during periods of
24
increased water temperature (Myers and Hershberger, 1991; Blanc et al., 1992; Ojolick et al.,
25
1995). In contrast, experimental studies designed to test the critical thermal maxima would
26
suggest there is no difference between triploid and diploid fish. For instance, the critical
27
thermal maxima of brook charr (Salvelinus fontinalis) was observed to be equal for under-
28
21
yearlings and yearlings after temperature increases of 2 and 15 ˚C h-1 (Benfey et al., 1997).
1
Similarly, no ploidy effects in juvenile rainbow or brook trout were recorded after a more
2
realistic life setting, whereby temperature was increased at a slower rate (2 ˚C day-1)
3
(Galbreath et al., 2006). However, when Atlantic salmon were reared in combinations of high
4
temperature and hypoxia, triploid mortality rates were significantly higher than in diploid
5
counterparts (Hansen et al., in prep) suggesting mortality is linked to issues relating to oxygen
6
delivery (Bernier et al., 2004) at high temperatures, not merely high temperature.
7
8
Limited evidence would suggest cardiac performance over various temperature ranges does
9
not appear to be affected by the triploid state. For example, in triploid brook charr embryo-
10
larval stages, heart rate increased with temperature but no effect of ploidy was observed
11
(Benfey and Bennett, 2009). Triploid perfused heart preparations displayed no difference in
12
maximal values for heart rate, stroke volume, or cardiac and myocardial power output at two
13
acclimation temperatures (14 an 18 ˚C) in triploid female brown trout (Mercier et al., 2002).
14
However, the latter study contained no diploid comparisons and there was a high mortality
15
amongst the experimental fish reared at 18 ˚C, possibly biasing the results towards an equal
16
performance. In addition, Merceir et al. (2000) reported heart rates in inactive triploid brown
17
trout that were high (85-100 % of maximal myocardial performance) and insensitive to
18
disturbances in high water temperatures (18 ˚C), though again, no comparisons were made
19
with diploids.
20
21
Dissolved oxygen
22
A large body of work has focused on oxygen delivery in triploid fish, and as yet there is little
23
evidence to suggest it is compromised compared to their diploid conspecifics without the
24
addition of temperature stress (see above). It was initially expected that as triploids possess
25
fewer yet larger erythrocytes this might affect oxygen carrying capacity, due to larger cell
26
surface areas effecting diffusion processes, but the majority of studies have found no ploidy
27
effect (Table 5). For instance, triploids are typically found to have similar heamatocrit,
28
22
haemoglobin, tissue oxygen unloading capacity, oxygen consumption rates, and critical
1
swimming velocity, and display no signs of increased use of mechanisms to alleviate inferior-
2
blood oxygen carrying capacity (with the possible exception of cardiac morphology, Leclercq
3
et al., 2011). However, a reduced factorial metabolic scope during swimming trials was
4
observed in triploid chinook salmon (Bernier et al., 2004) that is likely to be affected by
5
temperature (Altimiras et al., 2002).
6
7
Results on metabolic rates would suggest similar levels in triploids and diploids, though
8
again, results may be temperature dependent. For example, similar metabolic rates have been
9
observed in salmonids (Benfey and Sutterlin, 1984; Olive-Teles and Kaushik, 1990a, 1990b;
10
Bernier et al., 2004; Benfey and Bennett, 2009,) and the far Eastern catfish (Silurus asotus)
11
(Seol et al., 2008), although an exception has been reported (Stillwell and Benfey, 1996).
12
However, the results of Stillwell and Benfey (1996) could be explained by a ploidy
13
temperature effect. In Atlantic salmon and brook trout, triploids of both species had
14
significantly higher metabolic rates than diploids at lower temperatures (12 ˚C in both
15
species), and significantly lower metabolic rates than diploids at higher temperatures (18 and
16
15 ˚C in salmon and trout respectively, Atkins and Benfey, 2008). These results would match
17
the inverse relationship observed between metabolic rate and cell size that possibly relates to
18
the smaller surface area to volume ratios of larger cells reducing the metabolic cost per unit of
19
cell mass in maintaining ion gradients via membrane pumps (Lay and Baldwin, 1999).
20
21
Studies on post-exercise recovery suggest results are ploidy and temperature dependent.
22
Hyndman et al, (2003a) reported that diploid and triploid brook trout displayed a similar
23
metabolic response to exercise, but plasma osmolality, white muscle lactate and ATP levels,
24
as well as post-exercise oxygen consumption rates recovered earlier in triploids compared to
25
diploids. Further, it was observed that triploid brook trout excreted larger amounts of
26
ammonia following exhaustive exercise which may facilitate their recovery from acidosis, as
27
well as higher rates of ATP regeneration, clearance of white muscle lactate, and recovery of
28
23
ion and osmoregulatory imbalance through acid-base regulation. Recently, Lijalad & Powell
1
(2009) also suggested that triploid Atlantic salmon recovered better than diploids after
2
exercise, based on post-exercise oxygen consumption. However, at chronic high
3
temperatures, although triploid brook trout responded metabolically to exercise, the
4
magnitude of the response was different to diploids (Hyndman et al., 2003b). Triploids
5
suffered high mortalities (90 %) following exercise whereas diploids suffered no mortalities.
6
In addition, triploids used less phosphocreatine and more glycogen than diploids and had
7
difficulty utilising anaerobic pathways and clearing muscle lactate.
8
9
Several studies have suggested that triploid fish show a higher incidence of abnormal
10
erythrocytes in comparison to diploids. In triploid sturgeon Beyea et al. (2005) reported a
11
qualitative difference in the incidence of atypical red blood cells including dumbbell-shaped
12
(bilobed), teardrop-shaped and/or tailed cells, twisted cells, and plastid or anucleated cells in
13
triploids compared to diploids. These abnormal cells have been suggested to be indicative of
14
greater cellular division and a potential marker of stress (Houston, 1997). Other authors have
15
reported increased abnormalities and altered erythron profile related to triploidy in salmonids
16
(O'Keefe et al., 1999; Atkins et al., 2000; Dorafshan et al., 2008; Johari et al., 2008; Wang et
17
al., 2010) and Siberian sturgeon (Acipenser baerii) (Wlasow and Fopp-Bayat, 2011), along
18
with a lower osmotic fragility in triploid erythrocytes in shi drum (Umbrina cirrosa) (Ballerin
19
et al., 2004) and loach (Gao et al., 2007).
20
21
Hyperoxia
22
In the sole study regarding hyperoxia (150 460 % saturation) and triploid fish, triploid
23
rainbow trout were reported to display low (max 2%) yet higher levels of mortality than
24
diploids, where no mortalities were reported (Leggatt et al., 2006). In addition there was a
25
significant ploidy difference in hepatic glutathione (GSH) levels post stress, with lower
26
values in triploids, suggesting triploid fish had been subjected to oxidative stress more so than
27
diploids. These results could show triploids to be more susceptible to hyperoxic stress than
28
24
diploids, however, the authors could not rule out hypercapnia as the cause due to inefficient
1
water agitation.
2
3
Ammonia
4
The one study on ammonia toxicity in triploid fish reported a ploidy effect on the rate of
5
mortality but not overall mortality. In triploid and diploid South American catfish (Rhamdia
6
quelen) after a 96 hr exposure to a range of ammonia concentrations (0.8 3.4 mg l-1),
7
triploid fish displayed a greater sensitivity over the first 48 hrs and were suggested (not
8
quantified) to show a more passive behavioural response than diploids (Weiss and Zaniboni,
9
2009).
10
11
Salinity
12
The physiological response to seawater challenge and survival would appear to be similar
13
between triploids and diploids, even though triploid cells are suggested to have better
14
osmoregulatory capacity (Maxime and Labbé, 2010). Various physiological challenge tests to
15
evaluate the capacity of diploid and triploid fish to maintain ion and water balance have
16
demonstrated no significant differences between the two ploidy states. For example, no
17
differences were observed in levels of Na+/K+-ATPase activity in Atlantic salmon (Taylor et
18
al., in press), sea bass (Peruzzi et al., 2005), or non-smolting rainbow trout (Taylor et al.,
19
2007), plasma osmolality in salmonids (Johnson et al., 1986; Jungalwalla, 1991; Dumas et al.,
20
1995; Taylor et al., in press) and sea bass (Peruzzi et al., 2005), plasma chloride levels in
21
chinook salmon (Shrimpton et al., in press), or plasma sodium levels in sea bass (Peruzzi et
22
al., 2005). In contrast, Shrimpton et al. (2007, in press) observed triploid ocean-type chinook
23
salmon had reduced Na+/K+-ATPase activities compared to diploid counterparts, however, no
24
difference was observed in gene expression of Na+/K+-ATPase α1a or α1b. In addition,
25
cortisol levels were higher in triploids following a 24 hr seawater challenge in chinook
26
salmon, although no pre-challenge values were reported (Shrimpton et al., in press). Results
27
on seawater survival have shown either increased mortalities in triploid salmonids compared
28
25
to diploids (Galbreath and Thorgaard, 1995; McCarthy et al., 1996) or an equal performance
1
(Johnson et al., 1986; Bonnet et al., 1999; Shrimpton et al., in press). Where increased
2
mortalities are reported (Galbreath and Thorgaard, 1995; Withler et al., 1995), the reasons
3
remain unclear but could be due to researchers missing the smoltification window in triploids
4
or the size threshold value may be effected by ploidy (Galbreath and Thorgaard, 1995; Taylor
5
et al., in press). For instance, studies on Atlantic salmon have reported triploids to complete
6
smoltification 4 weeks earlier than diploids (Leclercq et al., 2011; Taylor et al., in press),
7
possibly due to the reported increase in size of triploid fish over diploids. However, both
8
these latter studies manipulated photoperiod to produce out-of-season smolts, whereas no
9
difference in smoltification time between diploids and triploids was observed in natural
10
seasonal smolts (Taylor et al., in press).
11
12
Photoperiod
13
Triploid Atlantic salmon performance was equal (survival and incidences of deformities) or
14
improved (growth) compared to diploid counterparts during exposure to continuous light and
15
simulated natural photoperiod (Oppedal et al., 2003) suggesting triploidy does not negatively
16
affect growth performance after increased daylength. After the onset of continuous light a
17
depression in feed consumption was noted during the first 6-8 weeks, but no ploidy
18
differences were documented. In addition, in Atlantic salmon, continuous day length is
19
effective in producing triploid out-of-season smolts as in diploids (Taylor et al., in press).
20
21
22
General summary
23
In summary, in terms of triploid welfare within aquaculture, the most significant finding is
24
that triploids have a higher prevalence of deformities and a reduced ability to withstand
25
temperature stress. However, the mechanisms that lead to increased deformity prevalence and
26
impaired high temperature tolerance in triploids are unknown. Ploidy has been demonstrated
27
to affect nutritional requirements and subsequently deformity prevalence in Atlantic salmon,
28
26
therefore, more work should focus on nutritional requirements in triploids. With regard to
1
temperature stress, triploid hypoxia tolerance and immunocompetence would appear to be
2
negatively affected by temperature increases, more so than in diploids. In addition, water
3
temperature is also linked to deformity prevalence in fish; therefore it becomes essential to
4
assess each new triploid species for temperature preferences and tolerable temperature
5
extremes. This is particularly important when comparing triploid to diploid performance.
6
Currently, triploids are consistently being compared to diploids under conditions that are
7
likely biased towards diploid performance.
8
9
Of specific concern, there is a general lack of information on the physiological performance
10
of triploids post release. Of those studies comparing triploid to diploid survival, a significant
11
number have found triploids to show higher rates of mortality within the wild, especially in
12
environments considered to be of poor quality (i.e. larger temperature fluctuations and periods
13
of low oxygen levels) although the underlying reasons remain unknown. It is likely that
14
triploids prefer a different temperature range to diploids. Supportive evidence for the reduced
15
tolerance of temperature extremes in triploids compared to diploids comes from the
16
observation that natural, self-sustaining populations of triploids are typically found further
17
north (in cooler climates) than the diploid colonies they originated from (e.g. Adolfsson et al.,
18
2010). Therefore, it is essential that in areas of intended triploid release, locations be assessed
19
on conditions tailored to triploid requirements. In addition, female triploid spawning
20
behaviour is impaired. These fish are not displaying normal behaviour, and the consequence
21
of this on fish welfare requires further evaluation. Finally, as triploid fish are commonly used
22
to stock sports fisheries, it is striking that we were unable to find a single study investigating
23
the stress response or survival post capture and release in triploid fish.
24
25
Future directions
26
As a consequence of this review, the authors would like to highlight the most important
27
directions for future research.
28
27
1
1. Currently, the most pressing area of concern in triploid welfare is the prevalence of
2
skeletal deformities, being higher in triploids compared to diploids. The mechanisms
3
behind this phenomenon are currently unknown. However, recent evidence suggests
4
triploids have different dietary requirements to diploids, and nutritional deficiencies
5
are a major cause of skeletal deformities. Another significant risk factor in deformity
6
incidence is water temperature, and triploids have different optimum temperature
7
ranges to diploids.
8
2. It seems likely triploids have different temperature optima than diploids, therefore it
9
is essential to determine the physiological effects of temperature on triploids.
10
Temperature at all life stages can influence the incidence of deformities,
11
cardiovascular performance (Farrell et al., 1996), the physiological response to stress
12
(Strange et al., 1977), and immunocompetance (Perez-Casanova et al., 2008).
13
Therefore temperature tolerance may be the underlying reason behind the previously
14
reported poorer performance of triploids compared to diploids in both the culture and
15
natural settings.
16
3. Further research is needed on evaluating differences in aggressiveness and social
17
behaviour between diploid and triploid fish. If indeed triploids are less aggressive
18
than diploids, this could improve the welfare of cultured fish in conditions where
19
social hierarchies are apparent (i.e. low stocking densities), as subordinate fish show
20
symptoms associated with chronic stress such as reduced growth, elevated stress
21
hormones, and impaired immune function (review, Gilmour et al., 2005).
22
4. A more comprehensive analysis of the stress response (both acute and chronic) is
23
required in triploid fish, especially in relation to common culture procedures such as
24
anaesthesia and sedation and high stocking densities.
25
5. There exists very little data on the nutritional requirements of triploid fish. The
26
dietary requirements of triploids are likely to differ from their diploid counterparts
27
due to differences in metabolic rates, ontogenetic growth, reproductive capabilities,
28
28
and incidence of deformities. In addition, many fish proteins and oils are now being
1
replaced with plant-based products where no data exists for triploids.
2
6. A number of current fish welfare aspects have not been investigated, both for the use
3
of triploids in aquaculture (including certain water quality parameters, stocking
4
densities, side-effects of vaccination, food withdrawal, and stress during slaughter)
5
and the use of triploids in fisheries management (including, social interactions with
6
wild fish, ability to adapt to the more complex natural environment, and the stress
7
response during capture).
8
9
A general consideration for all studies on the physiology of triploid fish is the importance of
10
sex on the parameters investigated, particularly in maturing fish. Gender has been
11
demonstrated to influence both the physiology and morphology of a number of organs and
12
processes in teleosts (review Hanson et al., 2008), including the stress response (Carragher et
13
al., 1989), immunology (Aaltonen et al., 2000), and heart (Davie and Thorarensen, 1997) and
14
brain ontogeny (Kolm et al., 2009), in addition to having effects on behaviour (Øverli et al.,
15
2006). The reasons behind these differences are not always apparent, but sex hormones may
16
play a significant role (i.e. Pottinger et al., 1995; Davie and Thorarensen, 1997). Therefore, in
17
female triploids that typically demonstrate significantly reduced sex hormone levels in
18
comparison to diploids, special attention should be paid to the impacts on physiology and
19
behaviour, especially during maturation and adulthood. The importance of investigating the
20
influence of gender on triploids is increased by culture practices that typically use all female
21
stocks (even when using triploids as males do mature) as a management tool to prevent
22
unwanted sexual maturation.
23
24
Conclusions
25
A review of the current literature highlights the necessity to include triploidy in welfare
26
considerations. Currently, triploid fish are assumed to have the same welfare requirements as
27
diploid fish without significant justification (other than acceptable growth and survival).
28
29
Without knowing the ideal range of environmental conditions for triploids, it is difficult to
1
compare the current welfare state relating to ploidy. However, although similar in many
2
aspects of physiology, triploids have fundamental differences in cell organisation that affects
3
their physiology and behaviour in comparison to diploids. Consequently, triploids would
4
appear to have a higher prevalence of deformities and are more sensitive to temperature stress
5
that impairs their overall fitness, and as such their welfare. To that end, if the application of
6
triploid fish for both aquaculture and restocking purposes continues, a better understanding of
7
the differences in physiological responses between the ploidy states is needed in order to
8
account for best welfare practices.
9
10
Acknowledgements
11
We thank the library staff at the Norwegian School of Veterinary Science (NVH) for their
12
assistance. In addition, NVH is thanked for financial support.
13
14
30
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64
Table 1. Indicators of fish welfare 1
Welfare index
Examples
Survival
Poor water quality, inadequate nutrition, and chronic stress can all lead to decreased survival (MacIntyre et
al., 2008).
Growth
Varies naturally but slow growth can be indicative of chronic stress (Pickering et al., 1991).
Food intake
Usually the first sign of stress in fish. It can be caused by acute stress, such as handling (McCormick et al.,
1998), or chronic stressers (Pickering, 1993).
Metabolism
Stress increases ventilation due to a higher oxygen demand (Handy and Depledge, 1999), stimulates a
proteolytic action on fish white muscle and changes in amino acid metabolism (Mommsen et al., 1999).
Osmoregulation
Stress can influence osmoregulation in fish (Bonga, 1997).
Acute stress response
Many factors can alter the acute stress response in fish, including poor water quality (Pickering and
Pottinger, 1987) and nutritional deficiencies (Montero et al., 2001).
Condition factor
Can be influenced by a wide range of factors (i.e. developmental stage and diet) but can be in response to
reduced feeding (Nicieza & Metcalfe, 1997), poor water quality (Lemariè et al., 2004), deformities
(Fjelldal et al., 2009), and nutritional deficiencies (Beaverfjord et al., 1998).
Behaviour
Stress causes excessive, or severely reduced, swimming activity (Cooke et al., 2000a), whereas parasitic
infections (Barber et al., 2000) and toxins (Little and Finger, 1990) can alter a variety of fish behaviours.
Morphological deformity
Deformities can be produced by poor water quality (Branson and Turnbull, 2008), temperature (Grini et al.,
2011), diet (Halver and Hardy, 1994), stocking density (Ellis et al., 2002), swimming activity (Kihara et
al., 2002) or lack of environmental stimuli (Kihslinger and Nevitt, 2006).
Injury
Fin injury and scale loss caused by poor stocking densities (Winfree et al., 1998), whereas slow wound
healing could be indicative of stress (Roubal and Bullock, 1988).
Disease
Poor water quality (Le Morvan et al., 1998), nutritional deficiencies (Pearce et al., 2003), and increased
stress levels (Pickering and Pottinger, 1989) can increase the levels of disease.
65
Reproductive performance
Is reduced by nutritional deficiencies (Izquierdo et al., 2001), chronic stress (Schreck et al., 2001) and
abnormal rearing conditions such as increased photoperiod (Trippel et al., 2008).
1 2
66
Table 2. Welfare considerations of wild fish 1
Welfare
consideration
Example
Predation risk
Within the wild, fish may encounter a number of different predators throughout their life cycle (Johnsson
et al., 1996).
Social interactions
Wild fish tend to live within groups of the same species, sometimes competing for the same resources or
working together (Metcalfe et al., 2003).
Suboptimal
environmental
conditions
Variables within the natural environment typically fluctuate over time (seasonal changes), with conditions
likely to deviate from the optima for the species. In addition, human activities (Sindermann, 1979; Dunier
and Siwicki, 1993) or naturally occurring events (Landsberg, 2002) may expose fish to a number of toxins
impacting upon fish health.
Disease
Wild fish typically encounter a number of diseases and/or parasites within the natural environment,
resulting in threats to their health (Hedrick, 1998).
Behaviour
Wild fish may display migratory, shoaling, and/or aggressive (territory defence, fighting for a mate)
behaviour (Brown and Laland, 2001).
Nutrition
Food sources may not be readily available throughout the life span; wild fish can undergo long periods
without food (Schwalme and Chouinard, 1999).
67
Capture and/or
release
Fishing activities can induce physical damage (Meka, 2004), a physiological stress response (Pankhurst
and Dedual, 1994), alterations in behaviour (Cooke et al., 2000b), increase predation risk (Dallas et al.,
2010), and mortalities (Bartholomew and Bohnsack, 2005).
1 2
68
Table 3. Behavioural comparisons between diploid and triploid fish 1
Behaviour
Species
Comparison
to diploids
Reference
Aggression
Atlantic salmon
<
Carter et al. (1994)
=
O'Keefe and Benfey (1997)
Chinook salmon
<
Garner et al. (2008)
=
Garner et al. (2008)
Rainbow trout
<
Wagner et al. (2006)
=
Wagner et al. (2006)
Brook trout
<
O'Keefe and Benfey (1997)
=
O'Keefe and Benfey (1997)
Siamese fighting
fish
<
Kavumpurath and Pandian (1992)
Food
consumption
Atlantic salmon
=
Carter et al. (1994)
<
Carter et al. (1994)
Rainbow trout
<
Kobayashi and Fushiki (1997)
2
3
69
Table 4. Comparison of the incidence of deformities between diploid and triploid fish 1
Deformity
Species
Comparison
to diploids
Reference
Skeletal
Jaw
Atlantic salmon
=
Oppedal et al. (2003)
>
Sutterlin et al. (1987), Jungalwalla (1991), McGeachy et al. (1996), O'Flynn et al.
(1997), Sadler et al. (2001), Lijalad and Powell (2009), Leclercq et al. (2011)
Hybrid Atlantic
salmon
>
Sutterlin et al. (1987)
Sea bass
=
Felip et al. (2001), Peruzzi et al. (2004)
Turbot
=
Cal et al. (2006)
Operculum
Atlantic salmon
=
Taylor et al. (2011)
Sea bass
=
Felip et al. (2001), Peruzzi et al. (2004)
Other
skeletal
Atlantic salmon
=
Oppedal et al. (2003), Taylor et al. (2011, in press)
>
Sadler et al. (2001), Powell et al. (2009), Leclercq et al. (2011), Fjelldal and
Hansen (2010)
Rainbow trout
>
Kacem et al. (2004)
Sea bass
=
Peruzzi et al. (2004)
Turbot
=
Cal et al. (2006)
Stinging catfish
>
Tiwary and Ray (2004)
Gill filament
Atlantic salmon
>
Sadler et al. (2001)
Cataract
Atlantic salmon
=
Oppedal et al. (2003)
>
Wall and Richards (1992), Oppedal et al. (2003), Leclercq et al. (2011)
Swim
bladder
Sea bass
=
Peruzzi et al. (2004)
Stinging catfish
>
Tiwary and Ray (2004)
Head region
Atlantic cod
=
Trippel et al. (2008)
70
Bighead carp
>
Tave (1993)
1
71
Table 5. Studies on oxygen carrying capacity in triploids 1
Measurement
Species
Comparison
to diploid
Reference
Haematocrit
Rainbow trout
=
Benfey and Biron (2000)
<
Virtanen et al. (1990)
Brook trout
=
Benfey and Biron (2000)
Shortnose sturgeon
<
Beyea et al. (2005)
Shi drum
=
Ballerin et al. (2004)
Haemoglobin
Atlantic salmon
<
Benfey and Sutterlin (1984), Graham et al. (1985), Sadler
et al. (2000b)
Transgenic Atlantic
salmon
>
Cogswell et al. (2002)
Chinook salmon
=
Bernier et al. (2004)
Coho salmon
<
Small and Randall (1989)
Caspian salmon
<
Dorafshan et al. (2008)
Rainbow trout
<
Yamamoto and Iida (1994)
=
Benfey and Biron (2000), Taylor et al. (2007)
Brook trout
=
Stillwell and Benfey (1996), Benfey and Biron (2000),
Hyndman et al. (2003b)
Shortnose sturgeon
=
Beyea et al. (2005)
Ayu
=
Aliah et al. (1991)
Shi drum
=
Ballerin et al. (2004)
Turbot
<
Cal et al. (2006)
Tissue oxygen unloading
capacity
Atlantic salmon
=
Sadler et al. (2000b)
72
Oxygen consumption rate
Chinook salmon
=
Bernier et al. (2004)
Ucrit
Atlantic salmon
=
Cotterell and Wardle (2004), Lijalad and Powell (2009)
Chinook salmon
=
Bernier et al. (2004)
Coho salmon
=
Small and Randall (1989)
Brook trout
=
Stillwell and Benfey (1996)
Metabolic rate
Atlantic salmon
=
Benfey and Sutterlin (1984)
<
Atkins and Benfey (2008)
>
Atkins and Benfey (2008)
Chinook salmon
=
Bernier et al. (2004)
Rainbow trout
=
Oliva-Teles and Kaushik (1990a, 1990b), Yamamoto and
Iida (1994)
Brook trout
=
Benfey and Bennett (2009)
<
Stillwell and Benfey (1996), Atkins and Benfey (2008)
>
Atkins and Benfey (2008)
Far Eastern catfish
=
Seol et al. (2008)
Opercular abduction rate
Brook trout
=
Stillwell and Benfey (1996)
Ayu
=
Aliah et al. (1991)
Tail beat frequency
Brook trout
=
Stillwell and Benfey (1996)
Heart rate
Brook trout
=
Benfey and Bennett (2009)
1
... This approach has clear relevance for Atlantic salmon, Salmo salar, for which genetic introgression of escaped farmed fish into wild populations is well documented (Glover et al., 2017;Wringe et al., 2018). However, for the most part, the salmon farming industry has been reluctant to adopt triploids for commercial production due to reduced performance compared to conventional diploids (Fraser et al., 2012;Benfey, 2016;Madaro et al., 2021). For instance, triploid Atlantic salmon are more prone to developing cataracts and spinal deformities (Fraser et al., 2012), although these specific issues can be addressed through appropriate diet formulation to increase histidine and phosphorus availability, respectively (Taylor et al., 2015;Fjelldal et al., 2016;Smedley et al., 2016;Sambraus et al., 2017a;Peruzzi et al., 2018;Smedley et al., 2018;Sambraus et al., 2020). ...
... However, for the most part, the salmon farming industry has been reluctant to adopt triploids for commercial production due to reduced performance compared to conventional diploids (Fraser et al., 2012;Benfey, 2016;Madaro et al., 2021). For instance, triploid Atlantic salmon are more prone to developing cataracts and spinal deformities (Fraser et al., 2012), although these specific issues can be addressed through appropriate diet formulation to increase histidine and phosphorus availability, respectively (Taylor et al., 2015;Fjelldal et al., 2016;Smedley et al., 2016;Sambraus et al., 2017a;Peruzzi et al., 2018;Smedley et al., 2018;Sambraus et al., 2020). ...
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Rising temperature leads to reduced oxygen solubility and therefore increases the risk of exposure to harmful hypoxic condition for fish in their natural aquatic environments and in aquaculture. The goal of this study was to determine whether acclimation to warmer temperature can improve high-temperature hypoxia tolerance in fish, using sibling diploid and triploid brook charr as the experimental model. Triploid fish are used for aquaculture and fisheries management because they are sterile, but they are known to have reduced thermal and hypoxia tolerance compared to conventional diploids. Fish were pre-acclimated to either 15 °C (optimum temperature for diploids) or 18 °C and then assessed for high-temperature hypoxia tolerance by rapidly increasing temperature to pre-determined levels (up to 30 °C), holding fish at these temperatures for one hour, and then using compressed nitrogen to drive oxygen out of the water. Hypoxia tolerance was expressed as both the oxygen tension at loss of equilibrium and the time taken to reach this endpoint following the start of the trial. Acclimation to 18 °C improved hypoxia tolerance at high temperatures but this advantage was lost after reacclimation to 15 °C. Although 18 °C acclimation improved the hypoxia tolerance of triploids, it remained inferior to that of diploids under identical test conditions. Somatic energy reserves (estimated as condition factor and hepatosomatic index), cardiac output (relative ventricular mass) and oxygen carrying capacity of the blood (hemoglobin concentration and hematocrit) did not markedly affect high-temperature hypoxia tolerance.
... Induction of triploidy may lead to poor performance and welfare of salmonids, particularly after transfer to seawater (Fraser et al., 2012;Madaro et al., 2021;Taranger et al., 2010), perhaps because of differences in environmental, physiological, and nutritional requirements of triploids in comparison to diploids. In Norway, poor welfare scoring of triploid salmon in sea cages has led the Norwegian Seafood Authority to impose a temporary moratorium on triploid salmon production and farming. ...
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Triploidy is induced in Atlantic salmon (Salmo salar) to produce sterile fish for genetic containment and to hinder early sexual maturation in farmed fish, but it can have unwanted negative effects on growth, health, and welfare. However, the growth and welfare of triploid fish may be improved by adjusting the rearing environment, feeding conditions and diets. This study evaluated physiological changes and used a suite of biomarkers to assess the potential impact of diet on growth and welfare of diploid and triploid salmon during the parr-smolt transformation. Diploids and triploids, held at low temperature, were fed a standard salmon feed or one with hy-drolyzed fish proteins thought to be suitable for triploid Atlantic salmon. Fish muscle was collected monthly from October to December (2454-3044 degree-days post-start feeding, ddPSF) for analysis of biomarkers, and the progress of the parr-smolt transformation was monitored using a seawater challenge test. Real-Time PCR and radioimmunoassay were used to assess growth and stress response biomarkers (expression of genes of the GH-IGF axis and HSP70; cortisol concentrations), and oxidative stress biomarkers of lipids (MDA) and proteins (AOPP) were assayed. Changes in the biomarkers were related to sampling time rather than being associated with diet or ploidy, and the changes were compatible with the progression of the parr-smolt transformation. Growth and expressions of the biomarkers in triploid Atlantic salmon were similar to those of their diploid counterparts, and there was no evidence that the rearing conditions employed in the study resulted in stress responses being elicited. Overall, the physiological indicators and biomarkers employed in this study did not point to there being any dietary effects on performance and welfare of diploid and triploid salmon that were undergoing parr-smolt transformation.