Heikki Hirvonen

Innate antipredator responses of Arctic charr (Salvelinus alpinus) depend on predator species and their diet

The ability to discriminate between more dangerous and less dangerous predators can have serious fitness advantages for fish juveniles. This is especially true for hatchery-reared fish young used for stocking, because their post-release mortality is often much higher than that of wild-born conspecifics. We tested whether two coexisting fish predators and their different diets induce innate behavioral responses in predator-naive Arctic charr (Salvelinus alpinus) young originating from an endangered hatchery-bred population used for re-introductions. We predicted the antipredator responses of charr to be stronger towards chemical cues of brown trout (Salmo trutta) and pikeperch (Stizostedion lucioperca) than towards odorless control water. More pronounced antipredator behavior was predicted in treatments with predators fed on charr than when their diet consisted of another sympatric salmonid, European grayling (Thymallus thymallus), or when they were food-deprived. The Arctic charr young showed strong antipredator responses in all brown trout treatments, whereas odors of the less likely predator pikeperch were avoided with conspecific diet only. Freezing was the most sensitive antipredator behavior, as it was completely absent in control treatments. We found considerable individual variation in the amount and strength of antipredator responses. Although almost half of the charr failed to show antipredator behavior towards the piscivores, those with the innate ability showed highly sensitive recognition of predator odors. Our results indicate that the innate antipredator behavior of the juvenile fish is already finely tuned to respond specifically to chemical cues from different fish predators and even their diets.

Significance of memory properties in prey choice decisions

Abstract To forage efficiently in a spatially and temporally heterogeneous environment requires that an individual’s information from the immediate past is combined with information from the more distant past to track environmental change. We made use of a model involving exponentially devaluating weights for past events to emulate behaviour of the individual’s memory. As the devaluation rate increases, more weight is given to the most recent events. First, performance of individuals with different memory properties was tested in simulations in which two prey types with different profitabilities were available in different proportions. In a structurally stable prey environment a low memory devaluation rate gave better estimation of prey proportions than a high memory devaluation rate. In a highly variable environment, on the contrary, individuals with high devaluation rate could more quickly correct their estimates as prey availability changed, although this was achieved with the cost of high error rate of the estimate. Second, the ability to reliably assess relative abundances of the prey types proved to increase an individual’s success in prey choice (according to the decision rules by the optimal prey choice model). Third, in further simulations individuals were allowed to adjust their memory devaluation rate according to experience from their success in prey choice decisions in previous patches. We found that there was no need to adjust a high devaluation memory in a highly variable environment, but foragers starting with low devaluation value rather rapidly shifted to high devaluation rates. In a relatively stable environment the situation was reversed and finally all foragers used low devaluation rates. These results imply that the variation in estimation efficacy of prey availability may be critical in terms of optimal prey choice and thus memory properties should be included in examinations of prey choice. Including individual variation in foraging performance in individual-based models could increase our understanding of the consequences of these differences at the population and community levels.

Less is more: social learning of predator recognition requires a low demonstrator to observer ratio in Arctic charr (Salvelinus alpinus)

Reintroduction programs for conservation purposes suffer from low post-release survival of captive-bred animals, especially so with fish reintroductions. High mortality is most often due to weakened antipredator skills, which could be enhanced through direct experience with predators and social learning. As yet, the relative efficiency of these learning methods has not been tested, and the significance of the factors determining how efficiently antipredator responses are transmitted socially from experienced (“demonstrator”) to predator naive (“observer”) individuals is largely unknown. Using hatchery-bred stock of the endangered Saimaa Arctic charr (Salvelinus alpinus), we show for the first time that: (1) contrary to theoretical predictions, acquired predator recognition was only socially transmitted from predator-experienced to predator-naive fish in groups with a smaller proportion of experienced than naive individuals, and that (2) socially acquired avoidance of the predator odors was as strong as in those fish conditioned with a combination of odors and predator exposure. We conclude that using social transmission procedures in training fish for reintroduction programs may provide considerable ecological, economical and ethical advantages.

Prey to predator size ratio influences foraging efficiency of larval Aeshna juncea dragonflies

We investigated foraging behaviour of larval dragonflies Aeshna juncea in order to examine the significance of prey density and body size in predator-prey dynamics. A. juncea were offered separately three size-classes of Daphnia magna at low and high densities. The data were collected with direct observations of the foraging individuals. We found that large A. juncea larvae could better enhance their intake of prey biomass as prey size and prey density increased than their smaller conspecifics. However, increasing feeding efficiency of both larval instars was constrained by declining attack success and search rate with increasing prey size and density. With small D. magna, in contrast to large A. juncea, small A. juncea increased their searching efficiency as prey density increased keeping D. magna mortality rate at a constant level. In a predator-prey relationship this indicates stabilizing potential and feeding thresholds set by both prey density and prey-predator size ratio. Attack success dropped with prey size and density, but did not change in the course of the foraging bout. For both A. juncea sizes prey handling times increased as more medium and large prey were eaten. The slope of the increase became steeper with increasing prey-predator size ratio. These observations indicate that components of the predator-prey relationship vary with prey density, contrary to the basic assumptions of functional response equations. Moreover, the results suggest that the effects of prey density change during the ontogeny of predators and prey.

Female and male contribution to egg size in salmonids

Egg size contributes to other life history traits of an individual. It is traditionally considered as a maternally determined characteristic to which the male does not have any direct contribution. However, a recent finding in insects suggests that males can affect egg size also directly. In fish, the male effect could take place only during egg swelling, as the final egg size is reached after that. We studied egg size in four freshwater salmonid species (the land-locked Atlantic salmon, the brown trout, the Arctic charr and the lake trout) right after fertilisation (initial egg size) and after the swelling phase (final egg size). The results showed that the final egg size is affected not only by the initial egg size but also by both the female and the male through the process of egg swelling. This study suggests that paternal contribution may form a previously largely ignored source of variation in early life history traits in salmonid fish.

Boldness as a consistent personality trait in the noble crayfish, Astacus astacus

Consistent individual differences in behavioural responses to perceived predation risk may have extensive ecological and evolutionary implications. We studied the repeatability of boldness across time and its relation to resource holding potential in the noble crayfish, Astacus astacus L., using predator-naïve immature individuals. We followed individual’s shelter use both with and without exposure to the chemical and physical cues of predators, and with and without the presence of a conspecific. In addition, we examined if armament, i.e. relative chelae size, would be correlated with individual differences in behaviour. Individuals showed repeatable behaviours across time and context. Individuals that occupied the shelter in competitive dyadic tests also spent more time in the shelter during individual control observations, suggesting that boldness is a personality trait that does not necessarily relate positively to high resource holding potential in the noble crayfish. The relative size of chelae did not correlate with any of the measured behavioural variables. Our results suggest that boldness can be considered as individually consistent and ecologically important personality trait in the noble crayfish.

Sniffing the trade-off: Effects of eel odours on nocturnal foraging activity of native and introduced crayfish juveniles

Efficient predator avoidance has to be balanced with other fitness-related behaviours such as foraging. Many aquatic animals coexisting with predators can recognise them through chemical cues and respond adaptively. Invasive or introduced species may lack this ability which may result in competitive disadvantage in the presence of predation risk. We investigated behavioural responses of predator-naïve juveniles of two co-occurring crayfish species to chemical cues of European eel (Anguilla anguilla). The native noble crayfish (Astacus astacus) has a long coevolutionary history with eel in Finland and the introduced signal crayfish (Pacifastacus leniusculus) a short one. We found that in the presence of odours from food deprived eels, noble crayfish increased shelter use and reduced nocturnal foraging activity. In contrast, signal crayfish reduced shelter use and increased their foraging activity when exposed to eel odours. These results indicate that signal crayfish would face a stronger risk of predation in waters with eel but the risk is reduced by their overall higher tendency to stay in shelter at night.

Variation in Resistance to the Invasive Crayfish Plague and Immune Defence in the Native Noble Crayfish

Emerging diseases, such as the crayfish plague, are a worldwide problem with serious ecological and economic impacts. Under the framework of ecological immunology, we investigated whether variation in crayfish plague resistance, the indicators of immune defence (encapsulation response, phenoloxidase and lytic activity), and the exploration behaviour among four subpopulations of noble crayfish is explained by potential local adaptation through differences in crayfish plague history, or alternatively by geographical divergence in a large watershed. We examined whether the strength of immune defence is associated with survival and exploration behaviour. Survival time after experimental crayfish plague infection and phenoloxidase activity differed among the subpopulations of the watershed but did not reveal local adaptation to the disease. Increased investment in immune defence (i.e. encapsulation response) compromised survival time after infection, suggesting the self-reactivity costs of mounting a strong immune response. Exploration behaviour was negatively associated with phenoloxidase activity before and after immune challenge.

Maternal effects in vulnerability to eye-parasites and correlations between behavior and parasitism in juvenile Arctic charr

Abstract Hatchery‐reared fish show high mortalities after release to the wild environment. Explanations for this include potentially predetermined genetics, behavioral, and physiological acclimation to fish farm environments, and increased vulnerability to predation and parasitism in the wild. We studied vulnerability to Diplostomum spp. parasites (load of eye flukes in the lenses), immune defense (relative spleen size) and antipredator behaviors (approaches toward predator odor, freezing, and swimming activity) in hatchery‐reared juvenile Arctic charr (Salvelinus alpinus) using a nested mating design. Fish were exposed to eye‐fluke larvae via the incoming water at the hatchery. Fish size was positively associated with parasite load, but we did not find any relationship between relative spleen size and parasitism. The offspring of different females showed significant variation in their parasite load within sires, implying a dam effect in the vulnerability to parasites. However, the family background did not have any effect on spleen size. In the mean sire level over dams, the fish from the bolder (actively swimming) families in the predator trials suffered higher loads of eye flukes than those from more cautiously behaving families. Thus, the results indicate potentially maternally inherited differences in vulnerability to eye‐fluke parasites, and that the vulnerability to parasites and behavioral activity are positively associated with each other at the sire level. This could lead to artificial and unintentional selection for increased vulnerability to both parasitism and predation if these traits are favored in fish farm environments.

Endogenous Seasonal Variation in the Encapsulation Response of the Noble Crayfish (Astacus astacus)

Seasonality in the immune defence of invertebrates can coincide with environmental variation but whether it is endogenously regulated, via biological clocks, or affected by previous immune challenges remains unclear. Using the native noble crayfish (Astacus astacus) held under constant laboratory conditions for a year, we explored (1) potential endogenous seasonal variation in immune defence, i.e. the encapsulation response, (2) the potential positive effect of repeated challenges with a standardized immune insult in subsequent seasons, i.e. long-lasting immune priming, and (3) whether long-lasting immune priming is dependent on endogenous seasonality. Independent measurements of the encapsulation response in different seasons revealed significant variation and a decrease in autumn. This result indicates previously undetected endogenous seasonal variation in invertebrate immunity. The weaker immune defence observed in autumn, i.e. the reproductive season of crayfish, might be caused by a circannual clock. When corrected for endogenous seasonality, we found no evidence for long-lasting immune priming.