Iodine nutrition and toxicity in Atlantic cod (Gadus morhua) larvae

Abstract

Copepods as feed promote better growth and development in marine fish larvae than rotifers. However, unlike rotifers, copepods contain several minerals such as iodine (I), at potentially toxic levels. Iodine is an essential trace element and both under and over supply of I can inhibit the production of the I containing thyroid hormones. It is unknown whether marine fish larvae require copepod levels of I or if mechanisms are present that prevent I toxicity. In this study, larval Atlantic cod (Gadus morhua) were fed rotifers enriched to intermediate (26 mg I kg(-1) dry weight; MI group) or copepod (129 mg I kg(-1) DW; HI group) I levels and compared to cod larvae fed control rotifers (0.6 mg I kg(-1) DW). Larval I concentrations were increased by 3 (MI) and 7 (HI) fold compared to controls during the rotifer feeding period. No differences in growth were observed, but the HI diet increased thyroid follicle colloid to epithelium ratios, and affected the essential element concentrations of larvae compared to the other groups. The thyroid follicle morphology in the HI larvae is typical of colloid goitre, a condition resulting from excessive I intake, even though whole body I levels were below those found previously in copepod fed cod larvae. This is the first observation of dietary induced I toxicity in fish, and suggests I toxicity may be determined to a greater extent by bioavailability and nutrient interactions than by total body I concentrations in fish larvae. Rotifers with 0.6 mg I kg(-1) DW appeared sufficient to prevent gross signs of I deficiency in cod larvae reared with continuous water exchange, while modelling of cod larvae versus rotifer I levels suggests that optimum I levels in rotifers for cod larvae is 3.5 mg I kg(-1) DW.

Keywords: Cod larvae; Colloid goitre; Fish larvae; Iodine requirement; Iodine toxicity; Mineral interactions; Rotifers; Thyroid follicles; Thyroid hormones.

Figure 1. Cod larvae length and dry weight.

Length (Data set L; mm fish^-1, left y axis) and dry weight (Data set W; mg fish^-1, right y axis) of cod larvae fed control (□), MI (○) or HI (●) rotifers, from 5 to 30 dph. At 5 dph, data are mean ± SD of 2 analytical parallels for dry weight and mean ± SD (n = 30) for length. Data at all other dph are mean ± SD (n = 3) where n represents the average of 10 larvae tank^-1 measured for length, and a group of 47 to 520 larvae group weighed then counted to determine individual mass.

Figure 2. Essential micro element concentration in whole cod larvae.

Essential micro element concentrations (mg kg^-1 DW) in whole cod larvae fed either control (□), MI (○) or HI (●) rotifers, from 5 to 30 dph. Letters denote statistically significant differences in mineral concentrations between treatments at a given day (one-way ANOVA; p < 0.05). Data are mean ± SD (n = 3), except at 5 dph where data are mean ± SD of analytical parallels.

Figure 3. Essential macro element concentrations in whole cod larvae

Essential macro mineral concentrations (g kg⁻¹ DW) in whole cod larvae fed either control (□), MI (○) or HI (●) rotifers, from 5 to 30 dph. Letters denote statistically significant differences in mineral concentrations between treatments at a given day (one-way ANOVA, p < 0.05). Data are mean ± SD (n = 3), except at 5 dph where data are from a single analysis.

Figure 4. Cod larvae iodine concentration in relation to their feed.

Ratio of iodine concentration (mg kg^-1 DW) in cod larvae versus their diet (rotifer iodine levels (mg kg^-1 DW)). X axis is log transformed. Line represents best fit model (Morrison Ki, R² = 0.94). Data are mean ± SD (n = 9).

Figure 5. Cod larvae thyroid hormone levels and ratios.

Normalised mean thyroid hormone levels (NML) in cod larvae fed either control (□), MI (○) or HI (●) rotifers. Graph A is tri-iodothyronine (T₃), Graph B is thyroxine (T₄), while graph C is the ratio between the NML of T₃/T₄. Data are mean ± SD (n = 3) for all data points except controls at 30 dph which has an outlier removed in graph B and C (n = 2).

Figure 6. Cod larvae thyroid follicle morphology.

Thyroid follicle morphology in cod larvae fed either control (□), MI (○) or HI (●) rotifers. Graph A shows the total number of follicles per fish, Graph B is the total thyroid follicle volume per fish, Graphs C and D show the volume of colloid or epithelium per fish, Graph E shows the ratio between the colloid and epithelium volumes. Letters denote statistically significant differences between treatments per time point (one-way ANOVA, p < 0.05). Data are mean ± SD (n = 3) where n consists of the average measurements from two fish per tank at 19 and 30 dph, and one fish per tank at 37 dph.

Figure 7. Thyroid follicle sections from cod larvae.

Thyroid follicle section from cod larvae (37 dph) fed either control (A) or HI (B) rotifers. Sections are stained with toulidine blue. C; thyroid follicle colloid, E; example of thyroid follicle epithelium. Scale bars are 100 µm.