V. N. Mikheev

Ecological and behavioural influences on juvenile fish migrations in regulated rivers: a review of experimental and field studies

This paper reviews results of experimental and field studies of downstream migration of young fish carried out in the Institute of Ecology and Evolution (Russian Academy of Sciences) as a part of the research programme on fish behaviour and ecology. Studies of fish migrations have been dominated by descriptions of migratory routes and proximate control of orientation. Behaviour and ecological factors influencing variability of downstream migrations of fish larvae and fry are still poorly understood. Life cycles of most of freshwater fishes can be roughly considered as a sequence of “residential” and “migratory” phases. Migrating, or just moving between microhabitats, fish are especially vulnerable to various threats including impacts of water abstraction systems. Abiotic (water flow velocity, rheogradients, turbulence, visual habitat heterogeneity) and biotic (foraging conditions, predators, competitors and parasites) factors can cause changes in fish spatial distribution as well as shift from residential to migratory behaviour. From the viewpoint of fish protection, these changes are important not only in the vicinity of water abstraction sites, but also in more distant parts of the aquatic system that should be taken into account in long-term assessments of impacts of abstraction on fish populations in regulated rivers. Besides macro- and meso-scale impacts that affect fish migrations and spatial distribution, micro-scale habitat heterogeneity (hydrodynamic and visual) are important as factors triggering and controlling various aspects of young fish behaviour. Interactions of water abstraction zones with fish populations have to be analysed at ecological (meso-scale spatial overlapping and long-term dynamics) and behavioural (effects of micro-scale structures and events) levels.

Host searching in Argulus foliaceus L. (Crustacea: Branchiura): the role of vision and selectivity

In laboratory experiments the swimming behaviour of the ectoparasite Argulus foliaceus and its infection rates on juvenile perch (Perca fluviatilis) and roach (Rutilus rutilus) were examined. The highest infection rate and a preference for perch juveniles were obtained in darkness, the lowest infection rate and a lack of preference in the light, when aquaria with glass walls (high reflectivity) were used. In the light, when aquaria were lined with black plastic (low reflectivity) an intermediate level of infection for perch and the highest for roach was recorded. Under such conditions roach were significantly more heavily infected than perch; an attack rate 4 times greater was recorded for brighter (more reflective) roach juveniles than for perch. Within the aquaria with a low reflective interior parasites swam 4.4 times slower and were observed predominantly in the central area, while in the highly reflective aquaria fast swimming A. foliaceus were recorded mainly near the walls. The primary role of visual stimuli for the host search behavior of A. foliaceus in the light is suggested. Parasites can effectively use such stimuli only in the low reflective surroundings. Highly reflective glass aquarium walls produce numerous secondary local light sources, which cause fast, erratic parasite movements and prevent the efficient location of potential hosts.

Light-mediated host searching strategies in a fish ectoparasite, Argulus foliaceus L. (Crustacea: Branchiura)

Argulus foliaceus, an obligate fish ectoparasite, can search for its hosts in both light and dark conditions and uses vision in the light. We have examined what searching mode is used at night, when the infection rate was at its highest, and which stimuli produced by the fish are most important. A change of illumination produced a clear difference in the searching behaviour of adult Argulus females. The mean swimming speed and the area explored were 3-4 times higher in the dark, when the parasite employed a cruising search strategy. This changed to an ambush (hover-and-wait) strategy in the light. The swimming activity is accompanied by changes in metabolic costs; the activity of the electron transport system being approximately 25 % lower in the light. The most pronounced light-induced differences in host-searching behaviour took place in moderately hungry parasites (starved for 24-96 h). Less motivated (just having left a fish) or exhausted animals did not exhibit any clear differences in swimming speed. Among the external signals tested, fish smell, from both perch (Perca fluviatilis) and roach (Rutilus rutilus), induced an elevated swimming speed of the parasite. Periodic water movements caused similar but weaker effects. The effects of these stimuli were observed under both light and dark conditions. We conclude that host-searching behaviour of A. foliaceus is under internal (state of hunger) and external (illumination and host-induced signals) control and involves all its sensory equipment (vision, olfaction and mechano-reception). Perch (but not roach) reduced their swimming speed in the dark, which make them more susceptible to cruising Argulus. Thus the behavioural interplay between hosts and parasites can also influence the infection rate of A. foliaceus found on perch and roach in Finnish lakes.

Parasite-induced aggression and impaired contest ability in a fish host

BackgroundSuccess of trophically transmitted parasites depends to a great extent on their ability to manipulate their intermediate hosts in a way that makes them easier prey for target hosts. Parasite-induced behavioural changes are the most spectacular and diverse examples of manipulation. Most of the studies have been focused on individual behaviour of hosts including fish. We suggest that agonistic interactions and territoriality in fish hosts may affect their vulnerability to predators and thus the transmission efficiency of trophically transmitted parasites. The parasite Diplostomum spathaceum (Trematoda) and juvenile rainbow trout, Oncorhynchus mykiss, were used to study whether infection can alter aggression rates and territorial behaviour of intermediate fish hosts.ResultsThe changes in behaviour of rainbow trout, Oncorhynchus mykiss, infected with an eye fluke Diplostomum spathaceum (Trematoda), was monitored over the course of an experimental infection for 1.5 months. At the beginning of their development, not yet infective D. spathaceum metacercariae decreased the aggressiveness of rainbow trout. By the time that metacercariae were fully infective to their definitive hosts, the aggressiveness increased and exceeded that of control fish. Despite the increased aggressiveness, the experimentally infected fish lost contests for a territory (dark parts of the bottom) against the control fish.ConclusionsThe results obtained indicate that the parasitized fish pay the cost of aggressiveness without the benefit of acquiring a territory that would provide them with better protection against predators. This behaviour should increase transmission of the parasite as expected by the parasite manipulation hypothesis.

Changes in host behaviour caused by immature larvae of the eye fluke: evidence supporting the predation suppression hypothesis

The manipulation of host behaviour by the not-fully-developed, immature larvae of trophically transmitted parasites is attracting growing interest. A theoretical model predicts that while facilitation of host predation risk is advantageous for fully developed parasite larvae, the immature ones should make hosts less vulnerable to the predators (predation suppression hypothesis). However, there is still little evidence of such manipulation by non-infective parasite stages. We tested whether immature trematode larvae of the eye fluke, Diplostomum pseudospathaceum, a common parasite of many freshwater fishes, enhance the anti-predatory responses of their host (Oncorhynchus mykiss). To test the predation suppression hypothesis, we experimentally infected young-of-the-year (YOY) rainbow trout and studied the influence of pre-infective metacercariae of the eye fluke on the anti-predator behaviour of the fish. Fish activity, depth preference and the ability to avoid simulated predation were evaluated in the experiments. Infected fish—harbouring a moderate number of immature metacercariae—were significantly less vulnerable to simulated predation (dip-net catch) and less active (horizontal move), but their swimming depth (vertical position) was not changed when compared with the control fish harbouring no larvae. Our findings suggest that immature larvae of D. pseudospathaceum induce changes in host behaviour that can protect them from predation, thereby supporting the predation suppression hypothesis and indicating that manipulations caused by immature parasites may play an important role in modulating predator–prey interactions.

Contestable shelters provoke aggression among 0+ perch, Perca fluviatilis

SynopsisWe examined behavioural interactions and feeding within triads of young-of-the-year (YOY) Eurasian perch, Perca fluviatilis, in aquaria with and without a shelter. For the first time we showed that competition for shelters, but not for food, provokes aggressiveness and triggers establishment of social hierarchy among young perch. No aggressiveness occurred during feeding bouts, when food was a limited resource. We expect the observed interactions to occur in natural heterogeneous habitats providing limited number of refuges and high local density of fish. They may ultimately lead to previously anticipated interference competition among juvenile perch.

Grouping facilitates avoidance of parasites by fish

BackgroundParasite distribution is often highly heterogeneous, and intensity of infection depends, among other things, on how well hosts can avoid areas with a high concentration of parasites. We studied the role of fish behaviour in avoiding microhabitats with a high infection risk using Oncorhynchus mykiss and cercariae of Diplostomum pseudospathaceum as a model. Spatial distribution of parasites in experimental tanks was highly heterogeneous. We hypothesized that fish in groups are better at recognizing a parasitized area and avoiding it than solitary fish.MethodsNumber of fish, either solitary or in groups of 5, was recorded in different compartments of a shuttle tank where fish could make a choice between areas with different risk of being infected. Intensity of infection was assessed and compared with the number of fish recorded in the compartment with parasites and level of fish motility.ResultsBoth solitary fish and fish in groups avoided parasitized areas, but fish in groups avoided it more strongly and thus acquired significantly fewer parasites than solitary fish. Prevalence of infection among grouped and solitary fish was 66 and 92 %, respectively, with the mean abundance two times higher in the solitary fish. Between-individual variation in the number of parasites per fish was higher in the “groups” treatment (across all individuals) than in the “solitary” treatment. Avoidance behaviour was more efficient when fish were allowed to explore the experimental arena prior to parasite exposure. High motility of fish was shown to increase the acquisition of D. pseudospathaceum.ConclusionFish in groups better avoided parasitized habitat, and acquired significantly fewer parasites than solitary fish. We suggest that fish in groups benefit from information about parasites gained from other members of a group. Grouping behaviour may be an efficient mechanism of parasite avoidance, together with individual behaviour and immune responses of fishes. Avoidance of habitats with a high parasite risk can be an important factor contributing to the evolution and maintenance of grouping behaviour in fish.

Combined effects of predators and parasites on shoaling behavior of fishes

A review of experimental, field and theoretical papers on several topics related to the study of variability of fish shoaling behavior caused by separate impacts of predators and parasites as well as by combined effects of these factors. First, antipredator functions and changes in fish shoal parameters caused by predation risk are briefly discussed. Then, effects of parasites that have the potential to act as a force that can select for either larger or smaller group size, or even for solitary behavior are reviewed. Predation- and parasitism-induced variations in the shoal size and shape, distance between members of a shoal, position of fish within a shoal, effects of habitat complexity, parasite-assortative shoaling are described. Finally, an interplay between the parasitism and predation risks that could influence protective functions of fish shoaling is discussed. It is emphasized that not only the binary “predator-prey” and “host-parasite” systems, but a three-component system “parasite.-host-predator” which embrace both direct and indirect effects have to be studied.

Swimming response of goldfish, Carassius auratus, and the tetra, Hemigrammus caudovittatus, larvae to individual food items and patches

SynopsisSwimming speed and swimming path of goldfish and tetra larvae were studied in aquaria containing food patches composed of decapsulated cysts and immobilized nauplii of Artemia salina or sparsely distributed prey. The mean swimming speed of starved larvae in the medium without food was about four times higher than the speed of larvae feeding in a patch. Satiated larvae swam about 1.5 times slower than hungry fish. Consumption of single prey items by starved larvae caused the following sequence of swimming responses: ‘handling pause’ (cessation of swimming), slow swimming in a restricted area, and fast swimming (approximately twice as fast as hungry larvae before encountering food) accompanied by a widening of the area searched (‘area increased searching’). Mean swimming speed was constant over a broad range (101–103 ind·1−1 of food density, although at extreme (high or low) values of food density it depended on swimming responses of the predator. Frequency of visits to the different parts of the aquarium strongly depended on encounters of hungry fish with food particles or patches.

Defense behavior of fish against predators and parasites

This paper is a review of empirical and theoretical studies of the behavioral mechanisms and ecological consequences of the anti-predator and anti-parasite activities of teleost fishes. While the individual and cooperative behaviors used by fish to protect themselves from predators have received marked attention from researchers in the fields of ecology, ethology and applied fish biology, the behaviors by which fish protect themselves from parasites have been poorly investigated. Generally, free-swimming parasites, which are difficult to distinguish, do not elicit any marked behavioral response from fish prior to contact. We hypothesize that the behaviors by which fish avoid parasites are much more efficient for fish in groups than they are for solitary fish. Early avoidance of predators and parasites is compared with the behavioral tactics fish use when such enemies are in close proximity. Individual versus cooperative tactics, as well as the role of learning, are also analyzed. Learning is more important for behaviors which protect fish from predators than those which they use against parasites, especially at the level of individual fish. Finally, we briefly discuss the importance of coordination of anti-predator and anti-parasite activities, which present the most complicated tasks for fish and intriguing problems for researchers.