Shelters can negatively affect growth and welfare in lumpfish if feed is delivered continuously

Introduction

Aquaculture is a growing industry and already now outcompetes fisheries as a source of seafood protein (FAO, 2016). Because of increasing demand, some sectors in the industry are under pressure to produce ever increasing volumes of food. The Atlantic Salmon (Salmo salar) farming industry is one of the sectors, where production has increased rapidly in recent years (FAO, 2016). The increased production is at risk of impacting fish welfare (Turnbull et al., 2005; Jansen et al., 2012). One of the problems in the North Atlantic stems from two parasitic copepods, Lepeoptheiris salmonis (salmon louse) and Caligus elongatus (sea louse). These parasites are often referred to collectively as ‘sea lice’ and they have a large impact on the salmon farming industry, causing huge economic losses (Costello, 2009; Abolofia, Asche & Wilen, 2017).

Salmon lice consume mucous, skin, and blood from salmon (Costello, 2006), causing sub-lethal injury to salmon and in extreme cases, mortality (Skilbrei et al., 2013). To avoid this impact on both salmon production and welfare, farming companies and governments alike implement a range of rules and methods to keep infestation levels low. Historically, louse control methods have mostly consisted of chemical treatments and management practices designed to lower exposure to lice. While management practices are mostly sound, lice have proven to grow resistant to chemotherapeutants soon after they become available on the market (Aaen et al., 2015), so industry has been forced to find new ways of preventing accelerating louse infestations.

Many of the new louse prevention or removal methods are physical in nature. They involve either preventing louse access to salmon by using fine mesh “skirts” on cages or making the salmon swim at depths below where most of the free floating lice are (Frank et al., 2014; Stien et al., 2016), or they involve treatments using fresh water, warm water or pressurised water to flush the lice off the salmon (Grøntvedt et al., 2015; Lekang, Salas-Bringas & Bostock, 2016). All of these treatment and prevention methods are at risk of causing reduced salmon welfare or financial losses to farmers. Skirts can cause poor oxygenation (Stien et al., 2012) and “taking the surface away” from the salmon prevents natural behaviours (Barber, 2007). The various mechanical delousing methods cause stress and injury with resulting low appetite and mortality (reviewed in Bui et al., 2017). Some more inventive methods include a laser removal tool (Beck, 2015; Dumiak, 2017) and vegetable supplements in the feed (Jodaa Holm et al., 2016; O’Shea et al., 2017), but these are not yet commercially viable products. Finally, salmon farmers have been using cleaner fish, first a range of wrasse species (Fam. Labridae) starting in the 1980’s (Bjordal, 1988; Deady, Varian & Fives, 1995; Skiftesvik et al., 2014) and more recently, lumpfish (Cyclopterus lumpus) (Imsland et al., 2014a; Eliasen et al., 2018). Despite their generally hardy nature, lumpfish mortality on farms has been high and efficiency variable (Powell et al., 2017).

Lumpfish are a sedentary species with little buoyancy control due to the lack of swim bladder (Davenport, 1985). They use a sucker to attach to smooth surfaces and will generally only swim when necessary to avoid danger or to forage for food (Williams & Brown, 1991). Lumpfish that clean salmon will approach docile salmon, search for lice on the salmon, and pick the lice that they find off the salmon (Video S1). This behaviour is quite energy intensive, especially during times with strong currents or waves. In general, approximately 10% of lumpfish can be expected to have recently consumed lice at any one point in time on the Faroe Islands, though this is highly affected by seasonal availability of plankton causing a shift from 0 to 5% of lumpfish consuming lice when planktonic prey is available, to 15–20% when no planktonic prey is available (Eliasen et al., 2018). There is also some question as to the reliability of using lice found in the stomach as an indicator of how many lumpfish consume lumpfish because digestion times vary (Eysturskarð, Johannesen & Eliasen, 2016). The nutritional needs of lumpfish are not well documented, but given their prey choice, it is unlikely that lice meet those needs. However, it is possible that lumpfish prefer planktonic prey because they can employ a sit-and-wait strategy when planktonic prey is plentiful and simply stay attached to their shelters until the prey floats by in the current. There is no indication that lumpfish body condition is affected by louse burden in a salmon farm (Eliasen et al., unpublished data), so it is unlikely that lice play a major role in terms of nutrition for lumpfish.

Lumpfish are generally considered to use shelters, mainly for two purposes. They hide in or under them as an anti-predator behaviour and attach to them to rest (Imsland et al., 2014b; Imsland et al., 2015). This second use is related to their lack of swim bladder and the fact that their near spherical bodies are not well suited for rapid continuous swimming (Davenport, 1985). Because of the dual use of shelters, efforts are made to create shelters in salmon cages that accommodate both needs. The first shelters commonly used were variations on artificial seaweeds similar to those used for wrasses (see Skiftesvik et al., 2013). These shelters provided excellent options for hiding, but were not sturdy enough to provide suitable resting space (verbal feedback from salmon farmers). Other shelters, made from hard plastic, have provided good rigid resting space but have not provided much in terms of hiding places, as they are usually flat vertical surfaces, (see also Imsland et al., 2015).

Feed and shelter for lumpfish can become limited resources on a salmon farm. Feeding practices for lumpfish usually involve automated feeders dispersing feed in a limited area, though some farms use manual feeding. When feed is delivered manually, this is usually done once or twice per day with large quantities of feed delivered alongside the cage net and near the shelters. The fish keeper will look out for the fish and deliver more feed where the fish can be seen approaching the feed. Lumpfish are a docile and easily tamed species, so will usually approach fish keepers when they notice them. Though there is very little literature on how to best feed lumpfish, there is some indication that meal-time or “pulse” feeding promotes growth (Brown, Wiseman & Kean, 1997) and a more efficient feeding behaviour with less time spent foraging. On the contrary, fish may spend more time foraging and less time resting if feed is delivered continuously within a small area (Killen, Brown & Gamperl, 2007). Lumpfish will consume free floating feed pellets as well as pellets lying on the bottom of the tank (A Johannesen, pers. obs., 2015 from the production at the Nesvík Marine Centre). If shelters are located in such a way that a trade-off between an ideal resting/hiding place and feed availability emerges, there is a risk of competition for the best locations both in terms of shelter and feed (Pulliam & Caraco, 1984; Williams & Brown, 1991). Because of the potential competition related to the two resources, shelters and food, it is possible that shelter availability may negatively affect lumpfish growth or welfare if feed is a limited or difficult resource to gain access to. However, it is not currently clear whether continuous automated feeding provides better feed availability than manual “mealtime” feeding in this situation.

The aim of this study is to investigate the effect of shelters and feeding methods on lumpfish welfare, expressed by growth, body condition, and fin health. We use a crossed design with shelter availability: “Shelter” or “No shelter” crossed with two feeding methods: “Manual feeding three times per day” and “Automated feeding every 10 min during the day”. We expect that a shelter has a positive effect on growth and welfare and that manual feeding provides better growth due to prolonged resting times in between feeds. We also expect that “fin health” will be negatively affected by access to a shelter due to competition for optimal resting spaces, which causes a higher concentration of fish in a small area.

Methods

Results

In the 28 days that the trial lasted, mean weight increased by 4.87 g ± 0.14 (Fig. 1). Feeding method and shelter availability interacted (Chi-squared_1,16 = 7.77, P = 0.005, Fig. 1). A post-hoc linear model revealed that the treatment group ‘shelter+automated’ had significantly lower increase in weight than all other groups (summary table comparison to ‘shelter+automated’; ‘shelter+manual’: t = 4.59, P < 0.001; ‘no shelter+automated’: t = 3.43, P < 0.001; ‘no shelter+manual’: t = 4.02, P < 0.001; model statistics: F_3,195 = 8.52, P < 0.001; Fig. 1).

Fin damage score improved significantly over the course of the experiment (Z =  −10.16, DF = 5, P < 0.001, Fig. 2) and the portion of fish with undamaged fins increased from 13% to 31% (Fig. 2). No effect of treatment was found on the fin scores at the end of the experiment (shelter: Z = 1.41, P = 0.158; feeding method: Z =  − 0.18, P = 0.854, Fig. 3).

Body condition at the end of the trial was significantly lower in tanks with a shelter compared to those without shelters (median body condition: 0.71 and 0.75 respectively; $X_{\mathrm{1,5}}^2=4.20$, P = 0.04) and significantly higher in tanks with manual feeding than in tanks with automated feeding (median body condition: 0.75 and 0.72 respectively; $X_{\mathrm{1,5}}^2=5.33$, P = 0.02). No interaction was found between the effects of treatments on body condition ($X_{\mathrm{1,6}}^2=1.80$, P = 0.18, Fig. 4).

Discussion

In this experiment, we find that both the availability of shelter and the way feed is delivered to lumpfish have consequences for growth and body condition. In terms of body condition, the availability of shelter and automated feeding both reduce body condition such that the group that had lowest body condition was the fish that were provided with a shelter and an automated feeder. In absolute growth, there is a slightly different story, because while shelter availability does seem to lower growth, this is outweighed by manual feeding so that the fish with a shelter available did not have a lower increase in body weight overall compared to fish that did not have a shelter. In terms of fin health, there is no difference between the treatments, but all treatments seem to have been better than conditions in the stocking tanks as fin health improved over time from before the experiment to after. Ordinarily, aggression would be expected to be higher at lower stocking densities, and since stocking density was lower in the trial tanks than in the stocking tanks, a slight degradation in fin health was expected due to aggression and competition for shelter space. Improved fin health suggests that aggression was less prevalent in the trial tanks than in the stocking tanks. There may be other explanatory factors not investigated here. The fish were housed in a recirculation system before the trial and it is possible that the bacteria in that system were inhibiting fin healing, but there were no obvious signs of infection in any of the fish.

It is clear from this experiment that care needs to be taken to ensure that a situation of competition does not occur as a result of feeding method or deployment of shelters. Because of the behavioural need for a resting place and shelter (Imsland et al., 2015), it is important that suitable shelter is provided in sufficient amounts. However, because of a potential for competition for ideal spots in the shelter, care needs to be taken to ensure that feed is delivered in such a way that fish are able to compensate for any extra energy used for competition with increased feed intake (however, see Millidine, Armstrong & Metcalfe, 2006; Finstad et al., 2007).

Though enough feed was provided to all tanks to satiate all fish in this experiment, the amount delivered each 10 min from an automated feeder was so small, that not all fish had access to feed at the same time. Though not verified through quantitative observations, it is likely that the fish resting closest to where the feed was delivered were the fish that were able to feed first on any given day, and that the rest of the fish would feed only when the first fish reached satiation. It is also possible that a different temporal divergence occurred where dominant fish were able to feed at what was perceived as a less risky time causing lower ranked fish to limit their time spent foraging (Alanärä, Burns & Metcalfe, 2001). If fish closest to the feed delivery point could eat to satiation first, it is likely that there was competition for the spot in the shelter that was closest to where the feed was delivered. The competition for this spot may have caused increased use of energy and therefore lower growth than in the tanks with no shelter, where the bare tank surface area was large enough for all ten fish to sit near the feed delivery point (compare for example Andrew et al., 2004).

There is evidence in the literature that aggression increases when stocking density is low (Brown, Brown & Srivastava, 1992; Jørgensen, Christiansen & Jobling, 1993). Stocking density in this trial was very low, approximately 400 g per cubic metre compared to common stocking densities of 10–15 kg per cubic metre or more (Hosteland, 2017). It is possible that these results would not be replicated in a system with high stocking density due to decreased opportunity to establish social rank with resulting privileged access to feed. Therefore, the effects found here may be much diminished in a lumpfish production environment. However, in a typical salmon farm, the density of lumpfish is even lower than in this trial, approximately 10 g per cubic metre. This is a natural consequence of their small size and low numbers in salmon cages of 25–30 thousand cubic metres. Therefore, it is possible that situations will arise where lumpfish are able to establish a territory in specific locations in a salmon cage. Considering the need to adequately feed lumpfish in salmon cages, ensuring that all the fish have access to enough feed should be prioritised. As it can be difficult to track lumpfish in a salmon cage, one solution may be to disperse the lumpfish feed using an automated feeder similar to the commonly used salmon feeders and provide an additional daily meal of manually delivered feed near the shelters. Placing the shelters so that the feed can be delivered near them easily is worthy of consideration. However, there are other important considerations in terms of shelter placement that take priority over ease of feed delivery; these considerations being wave and sea current direction as well as shelter cleaning or maintenance.

In conclusion, while shelters can offer the necessary enrichment to meet the behavioural needs of lumpfish, careful planning is necessary when feeding methods are decided on. Growth is not necessarily a desirable lumpfish trait in a salmon cage, but body condition certainly is important for their welfare and survival. Similarly, for lumpfish producers, being able to provide optimal conditions for high growth allows producers to deliver lumpfish to salmon farms at a higher rate. Therefore, based on the results from this experiment, we cautiously recommend that feed is delivered in meal times in such quantities that all fish are able to feed simultaneously, especially in lumpfish rearing facilities. In salmon farms, manual feeding is best combined with automated pulse feeding using a feeder that disperses feed well. This ensures that feed is delivered when manual feeding is impractical, such as in bad weather or when days are much longer than working hours for staff.

Supplemental Information