Cohabitation With Atlantic Salmon (Salmo salar) Affects Brain Neuromodulators But Not Welfare Indicators in Lumpfish (Cyclopterus lumpus)

Abstract

Lumpfish are utilized to combat ectoparasitic epidemics in salmon farming. Research gaps on both cleaning behavior and client preferences in a natural environment, emphasizes the need to investigate the physiological impacts on lumpfish during cohabitation with piscivorous Atlantic salmon. Lumpfish (39.9 g, S.D ± 8.98) were arranged in duplicate tanks (n = 40 per treatment) and exposed to Live Atlantic salmon (245.7 g, S.D ± 25.05), salmon Olfaction or lifelike salmon Models for 6 weeks. Growth and health scores were measured every second week. In addition, the final sampling included measurements of neuromodulators, body color, and plasma cortisol. A stimulation and suppression test of the hypothalamic-pituitary-interrenal (HPI) axis was used for chronic stress assessment. Results showed that growth, health scores, and body color remained unaffected by treatments. Significant reductions in levels of brain dopamine and norepinephrine were observed in Live compared to Control. Plasma cortisol was low in all treatments, while the stimulation and suppression test of the HPI axis revealed no indications of chronic stress. This study presents novel findings on the impact on neuromodulators from Atlantic salmon interaction in the lumpfish brain. We argue that the downregulation of dopamine and norepinephrine indicate plastic adjustments to cohabitation with no negative effect on the species. This is in accordance with no observed deviations in welfare measurements, including growth, health scores, body color, and stress. We conclude that exposure to salmon or salmon cues did not impact the welfare of the species in our laboratory setup, and that neuromodulators are affected by heterospecific interaction.

Keywords: Atlantic salmon; aquaculture; cleaner fish; habituation; lumpfish; neuromodulators; welfare.

FIGURE 1

Specific growth rate (SGR % day^–1) in lumpfish (n = 40 per treatment) during 6 weeks of interaction with Live, Model or Olfaction treatments or Control. Mean measurements with 95% confidence interval error bars revealed no difference between treatments measured every second week, including an overall measurement comparing initial weight with endpoint weight.

FIGURE 2

Lumpfish skin color (n = 24) measured as mean Red + Green + Blue pixels (A) before and (B) after treatment exposure. Mean R + G + B did not deviate between treatments before or between treatments after the experiment. Lumpfish were reared in experimental tanks with Live Atlantic salmon or different salmon sensory cues (Olfaction and Model). Boxplots describe median values with quantiles and outliers.

FIGURE 3

The levels of neurotransmitters (ng g^–1) in ft hemisphere of brains from lumpfish (n = 12) exposed to Live, Model, or Olfaction treatments in addition to a Control. Neurotransmitters include (A) DA (dopamine), (B) DOPAC (3,4-dihydroxyphenylacetic acid), (C) the DOPAC:DA turnover ratio, (D) 5HT (serotonin), (E) 5HIAA (5-hydroxyindoleacetic acid), (F) the 5HIAA:5HT turnover ratio, and (G) NE (Norepinephrine). Treatments that share a letter were not significantly different (p < 0.05).

FIGURE 4

Mean basal plasma cortisol (nM) levels with 95% confidence intervals in lumpfish (n = 24) after 6 weeks of treatment exposure. Treatments involved interaction with two Atlantic salmon (Live), two salmon models (Model) or salmon smell from a tank containing four Atlantic salmon (Olfaction).

FIGURE 5

Mean plasma cortisol (nM) levels with 95% confidence intervals in lumpfish (n = 16) 2 h post-intraperitoneal injection with either 0.5 mL kg^–1 phosphate-buffered saline (PBS) or 45 μg mL^–1 adrenocorticotropic hormone (ACTH). 24 h prior to sampling, lumpfish were injected with 1 mg kg^–1 dexamethasone in ethanol: PBS; 1:3; 1 μg L^–1 (DEX) and relocated to dark tanks with the same environmental conditions as during the experiment. Treatments involved interaction with Live Atlantic salmon, salmon Models or salmon smell from a tank containing four Atlantic salmon. Treatments that share a letter were not significantly different (p < 0.05).