The effect of macroalgal, formulated and combination diets on growth, survival and feed utilisation in the red abalone Haliotis rufescens

doi:10.1016/j.aquaculture.2015.06.016

Aquaculture

Volume 448, 1 November 2015, Pages 306-314

https://doi.org/10.1016/j.aquaculture.2015.06.016 Get rights and content

Highlights

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We tested the effect of diet on the performance of Haliotis rufescens.
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A high macroalgae combination diet outperformed formulated feed.
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Increasing formulated feed contribution to diet increased canned meat yield.
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Macroalgae combined with formulated feed (FF) enhances the PER of the FF component.
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Provides a case for feeding combination diets in the production of red abalone.

Abstract

Abalone aquaculture in Chile is dominated by production of the red abalone Haliotis rufescens using a diet comprised predominantly of fresh, wild-harvested macroalgae. Concerns over the long-term supply of macroalgae have led farmers to investigate the suitability of various formulated feeds, however there has been limited commercial adoption. Combination diets of macroalgal and formulated feed fed together provide a mechanism to explore and adapt to formulated feed use without entirely abandoning macroalgal feed. The current study evaluated the use of formulated, macroalgal and two combination diets (low and high macroalgal supplementation) on production indicators and canning yields of juvenile abalone H. rufescens in a culture system modified for formulated feed. The macroalgal diet and the high macroalgal-formulated pellet combination diet (76.1% macroalgae: 23.9% pelleted diet as dry weight) produced significantly higher growth indicators (SGR and LGR) than the low macroalgal-formulated pellet combination diet (31.6% macroalgae: 68.4% pelleted diet as dry weight) and the formulated pellet diet. The protein efficiency ratio of the experimental treatments was positively related to the proportional contribution of fresh macroalgae in the diet. Furthermore, calculation of the protein efficiency ratio of the formulated component in combination diets (PER^f) revealed a significant positive relationship between macroalgae contribution and PER^f. This suggests that the increase in total PER is driven by the increased utilisation of protein in the formulated component of combination diets associated with increasing levels of fresh macroalgal supplementation. We suggest possible reasons why the presence of seaweed increased the availability of the formulated feed protein to the abalone. A simulated canning trial highlighted a significant positive linear relationship between meat canning yield and the proportional contribution of formulated feed. This study highlights the value of combination diets as a tool for abalone producers to harness the potential production advantages of macroalgae while still accessing the processing benefits associated with nutrient dense formulated feed.

Statement of relevance

We believe that this manuscript describes novel insights into the efficiency of protein utilisation in juvenile red abalone fed combination diets as well as the effect of diet, particularly formulated feed inclusion level, on canned meat yields. This provides empirical information to inform commercial abalone farmers of H. rufescens when exploring dietary options for optimal culture.

Introduction

Fresh macroalgae is the primary feed source used on abalone farms in Chile. Farms in the North (Regions III–V) generally use four wild-harvested species namely Lessonia trabeculata, Lessonia berteroana, Lessonia spicata and Macrocystis pyrifera while those in the South in the vicinity of Chiloé rely predominantly on wild-harvested M. pyrifera, but utilise cultured Gracilaria chilensis during winter months (Flores-Aguilar et al., 2007) (Fig. 1). When surveyed in 2006, land-based farmers considered feed to be the dominant constraint to the development of the industry, expressing concerns over the medium to long-term supply of macroalgae (Flores-Aguilar et al., 2007). Following from this concern the majority of farmers, both land and sea-based, listed feed as the most pressing research requirement. In addition, despite the industry testing various formulated diets, both locally produced and imported, concerns over poor growth rates and price had resulted in limited commercial adoption (Enríquez and Villagrán, 2008, Flores-Aguilar et al., 2007).

The experience of Chilean abalone farms in substituting macroalgal feeds with a formulated feed has been mixed, with the nutritional quality of the formulated diets, water stability and culture system design influencing performance. Culture systems designed for macroalgal diets are generally not suited to formulated diets, and require modifications to facilitate feed presentation and associated alterations to husbandry practices. As Chilean farmers were reluctant to convert to pelleted diets, the option of combination diets (i.e., macroalgae and formulated feed fed together) thus provided a pathway for abalone farmers to explore the use of formulated feeds without abandoning macroalgal dietary options entirely. Combination diets allow for an extended weaning period to facilitate dietary switch and there is a growing body of literature to suggest that combination diets provide superior production outcomes when compared to single diets, either macroalgal or formulated (Dlaza et al., 2008, Durazo-Beltrán et al., 2003, Naidoo et al., 2006). The effect of diet on the growth of abalone in commercial culture must however always be balanced against its effect on the quality and yield of the final product. Diet has been shown to affect the taste, texture, chemical composition and colour of abalone meat (Allen et al., 2006, Bewick et al., 2008, Chiou and Lai, 2002, Smit et al., 2007, Smit et al., 2010). While some Chilean abalone farmers have been using combination diets since as early as 2006 (Flores-Aguilar et al., 2007), there is a paucity of information regarding the performance of these diets and their subsequent effect on yields of the dominant Chilean abalone export product, namely canned abalone.

Therefore, the aim of this study was to evaluate the effect of fresh macroalgal, formulated pellet and two combination diets (low and high macroalgae supplementation with formulated diet) on production performance indicators and canning yields of juvenile abalone Haliotis rufescens in a culture system modified for the use of formulated feeds.

Section snippets

Culture system and experimental animals

The experimental culture system consisted of a 5000 l fiberglass raceway (10 m × 1 m × 0.5 m) with a single inflow of seawater (2500 l·h^− 1) and formed part of the production infrastructure at the AWABI Abalone Production Centre, Universidad Católica del Norte, Coquimbo, Chile (29°57′S; 71°21′W). Mean incoming water temperature at the facility over the experimental period was 13.3 ± 0.3 °C (range: 12.7–14.5 °C). Eight plastic mesh baskets (800 mm × 300 mm × 450 mm) were suspended in the raceway, with each divided

Growth and nutritional indices

Abalone weight increased significantly for all treatments over the 162 day period of the growth trial with growth rates described by the exponential curves as follows: (PD) y = 1.1497exp(0.0049x), r² = 0.98, P < 0.05; (MD) y = 1.1163exp(0.0061x), r² = 0.97, P < 0.05; (CMH) y = 1.1165exp(0.0064x), r² = 0.99, P < 0.05 and (CML) y = 1.1492exp(0.0053x), r² = 0.97, P < 0.05 (Fig. 2). The homogeneity of slope model showed significant differences between treatments in the slopes of natural log transformed weight data plotted

Discussion

The study demonstrated that for juvenile abalone H. rufescens fed macroalgal diets, up to 24% of the total feed intake on a dry weight basis could be substituted with formulated feed without negatively affecting growth rates. In addition, the inclusion of formulated feed into the diet of the abalone positively influenced canning yields.

The growth rates of 34–49 μm·day^− 1 (initial shell length 20.6 mm) for abalone in this study fall within the range (15–198 μm·day^− 1; initial shell length 5.9–46.7 mm)

Acknowledgement

The authors would like to thank Franklin Pincheira, Rattcliff Ambler and Mauricio Lopez for their technical assistance with this research. This study was funded through financial and in-kind contributions from Marifeed (Pty) Ltd. and Universidad Católica del Norte. Mr Kemp was supported through scholarships from Rhodes University and the Skye Foundation and would like to acknowledge this support. Two anonymous reviewers are thanked for their valuable comments that greatly strengthened this

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Therefore, a low protein content is likely to be the major reason for abalone's lower growth rate when feeding on a single macroalga (Dang et al., 2011). Previous studies have shown that feeding a formulated diet with fresh macroalgae in combination resulted in improved growth rate of abalone compared to a formulated diet only diet (Kemp et al., 2015). Haliotis midae has also shown that combination diets consisting of fresh macroalgae and formulated diet outperform the formulated diet alone (Dlaza et al., 2008).
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According to Bansemer et al. (2016c), it is possible that abalone have limited capacity to digest cellulose and other non-starch polysaccharides which serve as major structural carbohydrates in terrestrial plants such as soybean meal and lupins. Greenlip Abalone are reported to possess digestive carbohydrase enzymes, at sufficient activities, capable of at least the digestion of complex macroalgal polysaccharides found in macroalgae cell walls; more so in G. cliftonii than Ulva sp. (Kemp et al., 2015; Bansemer et al., 2016b, 2016c). Additionally, bacteria within the digestive tract of abalone are also known to contribute to complex macroalgal polysaccharide breakdown (Erasmus and Coyne, 1997; Harris et al., 1998).
Macroalgae meal may provide a useful source of dietary energy for cultured abalone. The inclusion of dried macroalgal meals in formulated diets may also provide other benefits such as improvement in growth, health and survival. In this 92 d study, energy allocation in Greenlip Abalone, Haliotis laevigata, fed either a commercial diet, the control diet (0% macroalgae meal inclusion), or diets containing three inclusion levels (5, 10 and 20%) of either of two enriched macroalgae meals, Gracilaria cliftonii and Ulva sp., was investigated. Energy budget models, which also accounted for shell growth energy and mucus production energy, were determined for each diet. Results varied in relation to energy budget components and diets. Overall, abalone fed the enriched G. cliftonii ingested significantly more dietary energy and exhibited higher somatic growth energy compared to those fed the commercial diet, the 0% control diet or the enriched Ulva sp. diets. Additionally, ingested feed energy decreased while somatic growth energy tended to increase with increasing enriched G. cliftonii meal inclusion level. In contrast, inclusion at any level with enriched Ulva sp. meal did not result in an improvement of somatic growth energy compared to the commercial or the 0% control diet. For ingested feed energy, 20% enriched Ulva sp. meal inclusion resulted in significantly higher values compared to either the commercial diet, control diet or the two other enriched Ulva sp. meal diets. However, abalone fed the 20% dried Ulva sp. meal diet lost significantly more energy through faecal egestion than those fed the commercial or the 0% control diets, suggesting reduced diet digestibility with increasing enriched Ulva sp. inclusion. The majority of ingested feed energy was allocated to somatic growth across treatments, while shell growth energy accounted for the smallest proportion of the energy budgets. Results suggest that the inclusion of enriched G. cliftonii meal (10% inclusion optimum) in formulated diets for Greenlip Abalone has energetic benefits for feed utilisation and growth which may lead to improved business productivity. Inclusion of selected macroalgae species in formulated diets for abalone is an approach where the benefits from feeding live macroalgae can be successfully transferred into these diets.
Heritability of energy intake and allocation and their correlated responses to selection on growth traits in cultured juvenile and adult red abalone Haliotis rufescens
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The present result is potentially very significant for the profitability and sustainability of abalone farming, because two economically relevant aspects such as time to harvest and expenditure in food could be reduced through a selective program for red abalone. Most abalone farms use fresh seaweed (mainly kelp) as feed, but this resource is becoming quite limited because of overexploitation, and this constitutes a bottle-neck for increased abalone production (Troell et al. 2006; Cook 2014; Kemp et al. 2015). Thus, the possibility to reduce food intake by selecting abalones is also positive in terms of the sustainability of this culture.
Increasing abalone growth rates and their physiological efficiency in the use of energy through selective breeding could improve abalone production. High potential responses to selection for growth traits have been estimated in several abalone species; however, the genetic bases underlying individual differences in physiological performance are unknown. The aims of this study were to estimate the heritable variation of physiological traits associated with energy intake and allocation for the red abalone Haliotis rufescens; and the potential correlated responses to selection between growth and physiological traits at three developmental stages. Growth traits (shell length and width, and total mass) and physiological traits [energy intake, standard metabolic rate (SMR), and energy losses by ammonia excretion and feces] were measured in individuals belonging to 60 full-sib families in 2-years old juveniles, 3-y old young adults, and 4-y old near-harvest adult (n = 500–380 individuals/age; total n = 1300). Food intake showed significant h² in juveniles and young adults (0.37 and 0.14, respectively); but near zero h² in near-harvest adults. Variation in energy required for SMR showed low but significant h² (0.13) in young and near-harvest adults. Variation in energy lost through ammonia excretion showed significant h² in juveniles (0.33) and in near-harvest adults (0.14). Heritability for variation in the energy losses through feces was not significant. Heritabilities for growth traits were all moderate to high and significant for young and pre-harvest adults, but were not significant for juveniles. At the young adult stage, food intake was negatively and highly genetically correlated with each of the growth traits (−0.70 to −0.85); and at the near-harvest adult stage both SMR and ammonia excretion showed high-negative genetic correlations with each growth trait (−0.88 to −1.00). Thus, estimated correlated response to selection indicated that if selection was exerted for higher growth (choosing 5% best individuals), we would be indirectly selecting for abalones with lower food intake (correlated responses of −11 to −15%); or lower metabolic demands of (−14 to −24%), if the selection was applied to young or near-harvest adults, respectively. In turn, shell length could be enhanced up to 18% per generation. These results suggest that higher growth in red abalone is genetically associated with a more efficient use of food and a lower metabolic demand. The possibility to reduce food intake or metabolic demands by selecting for faster growing abalones would be a very positive development for the sustainability of this culture.
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Most of the research on incorporating seaweeds into livestock diets as a source of protein has focused on aquatic livestock, especially commercial marine herbivores that feed naturally on seaweeds (abalone and sea urchins). Seaweeds can provide complete or partial protein nutrition for abalone (Bautista-Teruel, Millamena, & Fermin, 2001; Bilbao et al., 2012; Kemp, Britz, & Aguero, 2015; Mulvaney, Winberg, & Adams, 2013; Viera et al., 2011), sea urchins (Cook & Kelly, 2007) and shrimp (Cruz-Suarez, Tapia-Salazar, Nieto-Lopez, Guajardo-Barbosa, & Ricque-Marie, 2009; da Silva & Barbosa, 2009; Felix & Brindo, 2013). In contrast, the inclusion of seaweed in diets of commercial fish (herbivores or carnivores) at levels greater than 10% results in reduced growth and feed utilisation (Table 2), although there are some promising results for tilapia (Stadtlander et al., 2013).
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The effect of macroalgal, formulated and combination diets on growth, survival and feed utilisation in the red abalone Haliotis rufescens

Highlights

Abstract

Statement of relevance

Introduction

Section snippets

Culture system and experimental animals

Growth and nutritional indices

Discussion

Acknowledgement

Aquaculture

J. Invertebr. Pathol.

Aquaculture

Aquaculture

Aquaculture

J. Exp. Mar. Biol. Ecol.

J. Sea Res.

Aquaculture

Aquaculture

Food Chem.

Aquaculture

Aquaculture

Aquaculture

Aquaculture

Aquaculture

Aquaculture

Aquaculture

Aquaculture

Aquaculture

Nutritional requirements and use of macroalgae as ingredients in abalone feed

Rev. Aquac.

Free amino acid and nucleotide concentrations in New Zealand Abalone (Paua), Haliotis iris, fed casein-based, macroalgal, or wild diets

J. Aquat. Food Prod. Technol.

Physicochemical factors of abalone quality: a review

J. Shellfish Res.

Bioenergetics

Fish Nutr.

Effect of commercial carotene pigments (astaxanthin, cantaxanthin and beta-carotene) in juvenile abalone Haliotis rufescens diets on the color of the shell or nacre

Vet. Mex.

Ecological and Chemical Responses of Macrocystis spp. (Phaeophycae) Under Primitive Harvesting Methods — The Pursuit of a Sustainable Method of Harvesting in N. Chile

Comparison of taste components in cooked meats of small abalone fed different diets

Fish. Sci.

Growth of juvenile abalone, Haliotis discus hannai Ino 1953 and Haliotis rufescens Swainson 1822, fed with different diets

J. Shellfish Res.

The determinants and measurement of abalone growth