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.

Interactions between two parasites of brown trout (Salmo trutta): Consequences of preinfection

“…It has been proposed earlier that the relationship between M. margaritifera glochidia and fish host is neutral or mutualistic (e.g., Ziuganov, ; Ziuganov et al., ), but our results provide evidence that the relationship at least moderately antagonistic. Therefore, our data is consistent with previous studies, which demonstrated that brown trout infected with freshwater pearl mussel glochidia perform generally worse compared to uninfected fish (Filipsson et al., ; Österling et al., ; Taeubert & Geist, ; Thomas et al., ). This is in line with the fact that freshwater pearl mussel glochidia grow intensively on the fish gills and obtain nutrients from their hosts (Denic et al., ).…”

“…More importantly, D. pseudospathaceum along with many other trophically transmitted parasite species (see Poulin, 2010 for the review) are able to manipulate host behavior predisposing fish to predation by the definitive host-fish-eating bird (e.g., Crowden & Broom, 1980;Gopko et al, 2015Gopko et al, , 2017Mikheev et al, 2010;Seppälä et al, 2004Seppälä et al, , 2008. Therefore, by increasing the probability of concomitant infection freshwater pearl mussel glochidia can hamper their hosts in more subtle ways than it was suggested earlier (Filipsson et al, 2017;Österling et al, 2014;Thomas et al, 2014) which are not easy to detect without conducting comprehensive experimentation.…”

“…The latter is perhaps more likely to be true since freshwater pearl mussel glochidia demonstrate more than sevenfold growth in the course of 8–10‐month development on the fish gills with a substantial nutrient transfer from fish to glochidia and a shift in the stable isotope composition during the mussel's development (Denic, Taeubert, & Geist, ). In addition, M. margaritifera glochidia cause a pronounced immune response in their hosts, increase metabolic rates and hematocrit levels and hamper swimming and respiratory performance in brown trout (Chowdhury, Salonen, Marjomäki, & Taskinen, ; Filipsson et al., ; Österling, Ferm, & Piccilo, ; Taeubert & Geist, ; Thomas, Taylor, & Garcia de Leaniz, ). Impairment of the respiratory capacity of host fish is especially important since gills can be a place where other infectious agents enter the host.…”

Early stages of Margaritifera margaritifera glochidiosis in Atlantic salmon: Morphopathological characterization

“…However, as a result of the early larval rejection, the parasitism was localized in clusters and below 300 glochidia/fish g, following the recommendations for artificial breeding of this naiad (Taeubert & Geist, ). Thus, the impaired respiratory function might be balanced and alleviated due to redistribution of blood flow to non‐affected gill regions (Booth, ) or other compensatory mechanisms (Filipsson et al, ; Powell, Nowak & Adams, ).…”

Effect of glochidia infection on growth of fish: freshwater pearl mussel Margaritifera margaritifera and brown trout Salmo trutta

“…A number of negative effects of M. margaritifera on its fish host have been described. M. margaritifera glochidia cause hyperplasia and fusion of gill filaments (Treasurer & Turnbull, 2000;Thomas et al, 2014), inhibit swimming capability and increase mortality (Taeubert & Geist, 2013), reduce foraging, activity and dominance success (Ö sterling et al, 2014;Filipsson et al, 2016), induce spleen enlargement and lessen mucous cells of gills (Thomas et al, 2014) and increase metabolic rate and level of hematocrit (Filipsson et al, 2017). Therefore, our hypothesis was that M. margaritifera glochidia infection is harmful, decreasing the growth of the fish host, brown trout.…”