Using physiology to improve the health and sustainability of cleaner fish (lumpfish) production

Abstract

The aquaculture industry is the fastest growing food sector globally and its sustainable growth is essential in tackling growing global food insecurity. As more species are farmed, either directly for consumption, or indirectly to enhance other farmed species (e.g. as biological control against parasites), farmers need to work with scientists to understand how to optimise the environment in which individual species are bred to improve growth and welfare. In this thesis, I look at how aquaculture relevant variations in carbonate chemistry (i.e. carbon dioxide (CO2) and alkalinity) impact the growth and acid-base blood chemistry of lumpfish (Cyclopterus lumpus), a cleaner fish used as biological control against salmon sea lice, and how lumpfish compare to other teleost species under similar environmental conditions. To do this, I gathered aquaculture relevant water chemistry data and used the results as the basis for various experimental treatments. Once exposed to the different water chemistries, I then took blood samples to understand the extent and rapidity that lumpfish could regulate their acid-base blood chemistry. I also investigated the scale of variation in water chemistry across different types of aquaculture system, both temporally (across multiple days or seasons) and spatially (within & between sites), and what the impacts of varying environments may be on the species bred within them. There are five main types of aquaculture system used to grow aquatic food products; artificial ponds, open water net cages, bivalve rope / bed culture, flow through systems, and land-based recirculating aquaculture systems (RAS). To optimise growth and welfare of farmed species, farmers must monitor and manipulate the environment where possible, however, in systems which are open to the environment, like open water net cages and mussel beds, farmers have little control over the environment. I found that temperature and carbonate chemistry can fluctuate (chapter 4) depending on the location and set up of the site, and the type of temporal sampling that occurred. RAS are closed off from the external environment, and therefore are more biosecure than other aquaculture systems, as water is treated using a series of filtration systems which remove suspended organic matter and reduce unwanted microbes from the water. Within land-based RAS, farmers have more control over the environment, however, due to the recirculation of water, high stocking density (therefore high levels of respiration), and high solubility of carbon dioxide (CO2), CO2 can build to levels > 6-times higher than end of century predictions (chapter 4). When CO2 dissolves in water, it hydrates to form a bicarbonate ion and a proton, reducing pH. In an attempt to raise seawater pH back to “normal” (~ 8.1), farmers within land-based systems such as RAS, will often add an alkali, however, this is rarely achieved, and results in a unique water chemistry of elevated CO2, reduced pH, and elevated alkalinity. I found that the two closed RAS sites sampled had alkalinity 1.8 – 4 times higher than that of other sampled sites which are more frequently replenished with clean seawater (e.g. mussel beds; chapter 4). Lumpfish are farmed within RAS, not as a food product, but to serve the salmon farming industry and act as cleaner fish, grazing sea lice off salmon. I found that when exposed to RAS-relevant elevated CO2 (~ 3,600 – 6,400 μatm) and alkalinity (~ 4,600 μmol/kg) (data from chapter 3 and chapter 4), growth is reduced by 26 % (chapter 3), compared with lumpfish raised in control conditions (~ 550 μatm, close to atmospheric CO2; ~ 2,500 μmol/kg alkalinity, close to open ocean alkalinity). Food conversion ratio (i.e. how efficiently food is converted to mass; low values are more efficient) increased by 63 %, incurring increased costs for farmers, as more feed is required for lumpfish to grow, and the time for lumpfish to reach deployment size will be extended. Once lumpfish reach deployment size, they are transported to salmon farms, a journey which can take several days. During this journey, I found that CO2 rises to > 11,000 μatm (chapter 3) which is likely higher than they have ever experienced. Due to the increase in CO2, lumpfish blood will be acidifying as CO2 follows its concentration gradient from the water into the blood via the gills. This reduces blood pH, which can disrupt physiological processes (e.g. metabolic and osmoregulation). To compensate for the CO2-acidosis and restore blood pH to normal (~ pH 7.7), I found that lumpfish, like other marine teleosts, rapidly accumulate bicarbonate in their blood (chapter 2 and chapter 3). When exposed to transport levels of CO2, lumpfish blood bicarbonate increased 4 times (~ 20 mmol l-1) that of control fish (~ 5 mmol l-1), to maintain normal blood pH. To find out how quickly lumpfish could pH regulate their blood, I exposed lumpfish to ~ 9,000 μatm and blood sampled a subset of fish over the course of ~ 4 hours. I found that lumpfish could fully recover blood pH within 4 hours (chapter 2), after a rapid pH decline from ~ 7.7 under control conditions, to ~ 7.4 after ~ 17 minutes exposure. To do this, their blood bicarbonate increased ~ 4.5-fold, from 4 mmol l-1 to > 17 mmol l-1, I also observed that lumpfish experienced an erythrocyte alkalosis when exposed to ~ 9,000 μatm, where pH increased from ~ 7.5 to ~ 7.65. Altogether, my results show that lumpfish fit with other marine teleosts in their rapid and complete restoration of blood pH after exposure to aquaculture relevant CO¬2 levels, however, their growth and ability to convert food to mass is reduced, likely costing farmers time and money. To further improve the sustainability of the aquaculture industry, and welfare of the animals being farmed, physiologists and farmers should continue to work together to optimise the aquaculture environments, first by understanding the variations and challenges for maintaining a stable environment, and also what unique conditions individual species and life stages require for good welfare and production.