Encystment of parasitic freshwater pearl mussel (Margaritifera margaritifera) larvae coincides with increased metabolic rate and haematocrit in juvenile brown trout (Salmo trutta)

Abstract

Gill parasites on fish are likely to negatively influence their host by inhibiting respiration, oxygen transport capacity and overall fitness. The glochidia larvae of the endangered freshwater pearl mussel (FPM, Margaritifera margaritifera (Linnaeus, 1758)) are obligate parasites on the gills of juvenile salmonid fish. We investigated the effects of FPM glochidia encystment on the metabolism and haematology of brown trout (Salmo trutta Linnaeus, 1758). Specifically, we measured whole-animal oxygen uptake rates at rest and following an exhaustive exercise protocol using intermittent flow-through respirometry, as well as haematocrit, in infested and uninfested trout. Glochidia encystment significantly affected whole-animal metabolic rate, as infested trout exhibited higher standard and maximum metabolic rates. Furthermore, glochidia-infested trout also had elevated levels of haematocrit. The combination of an increased metabolism and haematocrit in infested fish indicates that glochidia encystment has a physiological effect on the trout, perhaps as a compensatory response to the potential respiratory stress caused by the glochidia. When relating glochidia load to metabolism and haematocrit, fish with low numbers of encysted glochidia were the ones with particularly elevated metabolism and haematocrit. Standard metabolic rate decreased with substantial glochidia loads towards levels similar to those of uninfested fish. This suggests that initial effects visible at low levels of encystment may be countered by additional physiological effects at high loads, e.g. potential changes in energy utilization, and also that high numbers of glochidia may restrict oxygen uptake by the gills.

Keywords: Glochidia; Haematocrit; Host; Margaritifera; Metabolic rate; Parasite.

Fig. 1

Linear relationships between mass (ln-transformed) and a standard metabolic rate (SMR) (ln-transformed), b maximum metabolic rate (MMR) (ln-transformed) and c haematocrit (Hct), for naturally infested and uninfested brown trout. Parameter estimates (B) and their standard error (SE) for the linear regression analysis and their statistical significance (presented as t statistics along with their p value) are presented in the boxes to the right of the graphs, and asterisks denote redundant parameter estimate

Fig. 2

Effects of glochidia load on a standard metabolic rate (SMR), b maximum metabolic rate (MMR) and c haematocrit (Hct). Boxplots on the left-hand side of each figure show the distribution of values for uninfested fish, the whiskers span between maximum and minimum values, the box delimits the upper and lower quartile, and the horizontal bar within the box shows the median. In the right-hand scatterplots, showing data in relation to glochidia load, the lines show the local regression (LOESS), with 95% confidence limits in grey. All data was standardized for size by using residuals from the respective linear model presented in Fig. 1