Using integrative acid-base physiology to improve the efficiency and sustainability of fish production

Lead Research Organisation: University of Exeter
Department Name: Biosciences

Abstract

Feeding and digestion has been and continues to be extensively studied for both fundamental and applied purposes, in a range of species from all animal groups. The current proposal represents a novel area of research that offers a new integrative perspective on the otherwise well studied phenomenon of digestion. It also provides a previously unforeseen mechanism for improving the conversion of food-to-growth within the globally important aquaculture of trout and salmon. The potential for commercial application has generated an industrial partnership with Skretting, the largest trout feed producer in the UK and worldwide.

The proposal stems from our recent discovery in 2008 that a major phenomenon associated with feeding in mammals, the alkaline tide, also occurs in teleost (bony) fish, in which it had not previously been documented. The alkaline tide is a rise in blood bicarbonate (a base) and pH (i.e. more alkaline) lasting several hours following a meal, which results from the need to balance the secretion of acid into the stomach. This carries an energetic cost that we estimate to be between about 5 and 40 % (depending on buffer capacity of the diet) of the energy used by trout to digest a meal. The resulting acid-base disturbance in the blood will also result in a host of physiological consequences including potentially negative effects on respiratory gas exchange, salt and water balance, energy use that will ultimately limit food conversion efficiency and growth rates.

In trout one key response to this blood acid-base disturbance is to excrete the excess bicarbonate base into the external water (via the gills), a compensatory process that can last 36 hours. Any treatments that might either lessen the extent of the alkaline tide, or improve the recovery time, could be extremely valuable to the aquaculture industry. This is because such treatments would reduce the energetic costs for the fish (promoting faster growth rates), reduce the economic costs for the fish farmer, and also lessen the impact on increasingly expensive and hard-fought-for marine resources that are currently used to make fishmeal (the primary ingredient in commercial trout food).

The project will focus upon the physiological consequences and costs of the alkaline tide in rainbow trout, and specifically how this might influence the biological and economic efficiency of growth in aquaculture conditions. By understanding the physiological implications of the alkaline tide, and how they are affected by environmental and dietary variables, we should be able to understand how this varies in nature (with fishing feeding naturally on diets with very different buffer capacity), and also how to minimise the energetic costs for fish within aquaculture. We aim to study how the temperature and chemistry of freshwater the fish live in can influence their response and recovery time for the alkaline tide. We will also manipulate the diet to see if we can minimise the need for the fish to secrete acid in its stomach and minimising the alkaline tide, thus saving energy and optimising fish growth.

We will investigate these phenomena using experimental physiology under laboratory conditions at Exeter, as well as carrying out commercial-scale feeding trials at Skretting's under conditions similar to aquaculture, using novel feeds designed by Skretting's Aquaculture Research Centre in Stavanger, Norway.

Technical Summary

The alkaline tide is a post-prandial elevation of blood bicarbonate and pH that results directly from gastric acid secretion after feeding. Although well known in mammals this phenomenon has only just been documented in teleost fish in 2008. Despite its recent discovery, this is likely to be the most frequently experienced acid-base disturbance, given the ubiquity and frequency of feeding, and yet we know little of its physiological consequences.

This Industrial Partnership Award project with Skretting focuses upon:

1) physiological costs and consequences of the alkaline tide in rainbow trout,
2) the genes and proteins controlling homeostatic acid-base recovery processes following a meal.
3) ways in which gastric acid secretion and the alkaline tide may be manipulated to improve the biological and economic efficiency of fish growth in aquaculture,

We aim to test the following three hypotheses by integrating integrative physiology, targeted gene/protein expression, and commercial scale feeding trials:

Hypothesis 1: Key endogenous and exogenous factors (meal size, temperature and water chemistry) will affect the extent and duration of a post-meal alkaline tide and the associated physiological consequences (acid-base balance, blood O2 transport, metabolism etc.).

Hypothesis 2: A range of genes and/or their proteins that control acid-base and ion regulation (secondarily associated with feeding and digestion), will be dynamically regulated following a meal (in the gill, gut and kidney). The localisation and quantification of targeted genes and proteins related to this transport will reveal homeostatic systems that are vital for whole organism health.

Hypothesis 3: Energetic costs of gastric acid secretion and the alkaline tide will depend on the buffer capacity of the diet, which can be experimentally or commercially manipulated (e.g. through pre-titration with acid) to make major improvements in the efficiency of food conversion into growth.

Planned Impact

Types of Beneficiaries and How They Might Benefit:

Academia: Beneficiaries will include fellow researchers worldwide within integrative and comparative physiology, but also researchers within the fields of animal nutrition, and post-genomic technologies. The breadth of the data produced in Objectives 1 and 2 will be of interest to a broad range of physiologists, including those studying the respiratory, metabolic, acid-base and ionoregulatory functions in animals and their integration with feeding and energetics. The planned research should advance our fundamental understanding of these functions, and as such will be disseminated through international physiological conferences and the highest quality peer-reviewed journals within the field (e.g. American J. Physiology; J. Experimental Biology).

Business/Industry: The project will also potentially have direct and immediate economic benefits to the aquaculture industry and animal feed production companies both in the UK and globally. Objective 3 will establish the potential physiological costs and energetic benefits of manipulating environmental and dietary variables in trout. This will be done using laboratory experiments, but also commercial-scale feeding trials that will validate the potential for commercial application to improve feed conversion efficiency in aquaculture. This will be of great interest to the industrial partner company (Skretting, the largest trout and salmon feed company in the UK and the world), but also to the aquaculture industry and commercial feed suppliers generally. It will also be of interest to researchers and companies within the field of animal nutrition. This part of the project will therefore be disseminated through key international conferences in the field (e.g. International Symposium of Fish Nutrition and Feed) and the highest impact peer-reviewed journals oriented towards aquaculture and animal nutrition (e.g. Aquaculture; Aquaculture Nutrition; J. Nutrition; British J. Nutrition). The outcomes will additionally inform important non-academic audiences such as small scale fish farmers, through a variety of outputs. For example, Skretting publishes a company newsletter ("Outlook") 2 to 3 times per year, and we would also aim to publish popular science articles in the Trade magazines (e.g. Fish Farming International; Fish Farmer; Aquatic Expert).
Objective 3 also has the potential to make significant improvements to food conversion efficiency in fish. Even small % improvements in growth efficiency can generate significant economic and environmental benefits for aquaculture. This would in turn help reduce the need for increasingly expensive and diminishingly available marine resources that are used to make fishmeal, currently the main ingredient of fish food for trout and salmon aquaculture. Any reduction in the need for fishmeal, whilst maintaining the same fish production in aquaculture, would therefore have positive environmental benefits. For example, our modified diets are predicted to improve absorption of Phosphorous, which should simultaneously reduce the eutrophication problem created by aquaculture effluents which is a major environmental limitation of fish farms. Outputs that support this hypothesis will therefore be communicated through the appropriate channels (e.g. Environment Agency, Defra etc.) to promote such environmentally-friendly practices that may improve the long term sustainability of aquaculture.

General Public: Improved efficiency of fish production, should eventually have a knock-on effect on the retail price of fish ,which would benefit the general public as consumers of fish. For target fish like salmon and trout, this will be especially useful due to the health benefits of eating these "oily" fish.

Publications

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Middlemiss KL (2016) Effects of seawater alkalinity on calcium and acid-base regulation in juvenile European lobster (Homarus gammarus) during a moult cycle. in Comparative biochemistry and physiology. Part A, Molecular & integrative physiology

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Montgomery DW (2019) Rising CO enhances hypoxia tolerance in a marine fish. in Scientific reports

 
Description We confirmed that freshwater chemistry can have a large influence on physiological recovery following ingestion of a meal in fish. This potentially means that the site of fish farms will influence how well, or how quickly, fish can process a meal and the efficiency of their growth.

We also established that fish have the largest acid-base disturbance after a meal (the "alkaline tide") of any animal studied to date. This has further repercussions for oxygen delivery to tissues during the metabolically challenging post-prandial period.

We have also tested dietary modifications that produce significant changes in post-prandial metabolism and growth. The nature of this data is confidential as their is an industrial application.
Exploitation Route The outcomes of this BBSRC funded research have contributed to two further BBSRC-funded FLIP projects.
Sectors Agriculture, Food and Drink,Environment

 
Description BBSRC FLIP (Flexible Interchange Programme)
Amount £149,829 (GBP)
Funding ID BB/M017583/1 
Organisation Biotechnology and Biological Sciences Research Council (BBSRC) 
Sector Public
Country United Kingdom
Start 06/2015 
End 12/2016
 
Description BBSRC FLIP (Flexible Interchange Programme)
Amount £149,863 (GBP)
Funding ID BB/N013344/1 
Organisation Biotechnology and Biological Sciences Research Council (BBSRC) 
Sector Public
Country United Kingdom
Start 12/2016 
End 05/2018
 
Description The role of water chemistry in zebrafish welfare and reproducibility of research studies
Amount £351,653 (GBP)
Funding ID NC/S001123/1 
Organisation National Centre for the Replacement, Refinement and Reduction of Animals in Research (NC3Rs) 
Sector Charity/Non Profit
Country United Kingdom
Start 08/2018 
End 08/2020
 
Description Using physiology to improve the health and sustainability of cleaner fish (lumpfish) production for the salmon aquaculture industry
Amount £82,000 (GBP)
Funding ID 2071339 
Organisation Biotechnology and Biological Sciences Research Council (BBSRC) 
Sector Public
Country United Kingdom
Start 09/2018 
End 09/2022
 
Description Talk on "How water chemistry and feeding profoundly influence fish physiology" - followed by Q/A and discussion with aquaculture industry representatives 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Industry/Business
Results and Impact SUNDERLAND MARINE: MARINE INSURANCE UK
Event Risk Management for the Scottish Salmon Company
11 Feb 2020
"Recirculation Aquaculture Systems"
Venue: Scottish Association for Marine Science (SAMS), Oban.

A keynote talk followed by question/answer session with both the salmon producers and the aquaculture insurance company partners, regarding ways in which the industry can improve fish health and welfare, mitigate against adverse health outcomes, and improve the efficiency and sustainability of fish production. This has been followed up by several communications wishing to explore further ways of either funding future research, or directly influencing aquaculture practices.

Audience included representatives from:
The Scottish Salmon Company
Sunderland Marine Insurance UK
Dryden Aqua (water treatment company)
Nova Q (microbiological water treatment company)
Blue Unit (Danish water chemistry analytical company)
Year(s) Of Engagement Activity 2020
URL https://i.emlfiles4.com/cmpdoc/1/2/2/6/7/1/files/46264_447---oban-event-risk-management-programme---...