The effects of hybridization and parasite infection on predation survival and behaviour of endangered landlocked salmon – implications for genetic rescue

A prerequisite of genetic rescue in endangered and genetically depauperate populations is to pre-evaluate between possible pros and cons of hybridization for the life history and survival of the target population. We hybridized critically endangered Saimaa landlocked salmon (Salmo salar m. sebago) with one of its geographically closest relatives, anadromous Baltic salmon. In two experiments conducted in semi-natural streams during overwintering (at age 1.5 years) and in early summer (age 2+), we studied how hybridization and infection of eye parasites (Diplostomum pseudospathaceum) affected fish survival under predation from Northern pike (Esox lucius). Additionally, we recorded movements of the juvenile salmon to explore the effect of hybridization and infection on antipredatory behaviour (movement activity and habitat use). Among the uninfected groups, mortality of hybrid salmon was significantly lower (14.5%) compared to purebred landlocked salmon (37.2%), supporting a positive effect of hybridization under predation risk. This benefit, however, was removed by the parasite infection, which impaired vision and increased the susceptibility of fish to predation. The negative effects of infection were particularly pronounced in the anadromous salmon due to its lower infection resistance compared to the landlocked salmon. Hybridization per se did not affect activity levels of salmon, but overwintering activity correlated positively with eye cataract coverage, and summer activity was highest in anadromous salmon. These results demonstrate that controlled hybridization of a small animal population with a genetically more diverse population could entail both positive and negative implications, at least in the first crossbred generation.

Methods
In October 2018, we hybridized the critically endangered landlocked salmon of the Vuoksi watershed, Finland (Salmo salar m. sebago Girard, 1853) with a geographically close Baltic anadromous salmon (Salmo salar L. 1758, population spawning in river Kymijoki, Finland, but originally from river Neva, Russia). Parental fish consisted of 15 males and 15 females from both populations, with eggs from each female being fertilized with one male from its own population and the other part with one male from the other population. Correspondingly, equal portions of milt from each male were used to fertilize eggs of one female from its own population and of one female from the other population (n = 60 full-sibling families, 15 per crossing group). This resulted in four crossing groups: purebred landlocked salmon (LL×LL), landlocked salmon females crossed with anadromous salmon males (LL×BA, hybrid), anadromous salmon females crossed with landlocked salmon males (BA×LL, hybrid), and purebred anadromous salmon (BA×BA).

Thereafter, we conducted two experiments in semi-natural circular stream tanks (Fig. 1) to examine growth, predation-induced mortality and behavioural traits among the crossing groups. These experiments were conducted at two life stages: during overwintering (winter experiment, at age 1.5-2 years) and in early summer (summer experiment, at age 2+). In both experiments (winter and summer), half of the salmon were infected with the D. pseudospathaceum eye fluke on 20.2.2020 to explore how parasitism in a central sensory organ influenced the crossing groups. Fish were measured before the start of the winter experiment on 26.10.-27.10.2020 and before the start of the summer experiment on 25.-26.5.2021.

After measuring the fish were transferred into the shallow stream-section of the experimental tanks (Fig. 1) on the 27.10.2020 (winter experiment) and 27.5.2021 (summer experiment). Into the pool-sections of tanks J506, J507, J513 and J516 we transferred in the winter experiment two Northern pike (Esox Lucius Linnaeus 1758, common piscine predators of juvenile salmonids) and in the summer experiment three pikes per tank. Tanks J505, J508, J514 and J515 were control tanks without predators. The winter experiment was terminated after 154 days on 6./7.4.2021 and surviving fish were recorded and measured again. The summer experiment was terminated after 28 days on 28.6.2021 when mortality was estimated to be similar than in the winter experiment. In the summer experiment survivors were recorded but not measured.

Passive integrated telemetry (PIT) antennae were applied during the experiments to record the behaviour of individuals (i.e. activity and habitat use), both in the presence and absence of predators. PIT-antennae were started and gates opened 3.11.2020 (winter experiment) and 31.5.2021 (summer experiment), enabling the salmon to move to the potential predators on the pool-sides. In the winter experiments tanks J513 and J505 the gates had opened before the PIT antennae were started (PIT-data potentially unusable).

The study was conducted at the Kainuu Fisheries Research Station in Paltamo, Finland (64ᵒ24’N 27ᵒ31’E) maintained by the Natural Resources Institute Finland (Luke).