Fish Cues Research Articles

Depth distribution of Daphnia in response to a deep‐water algal maximum: the effect of body size and temperature gradient

Summary1. In the absence of fish predation, Daphnia exploiting a deep‐water algal maximum are faced with a trade‐off. They can either dwell in the epilimnion where development in the warm water is fast, but food shortage causes low egg production, or in the hypolimnion, where food availability is high but development is slow because of low temperatures.2. We tested the hypotheses that (i) depth distributions of various ontogenetic stages (size classes and egg‐bearing females) differ because daphnids react to light with size‐specific diel vertical migration (DVM) even in the absence of fish (residual predator avoidance hypothesis) and (ii) differently sized daphnids select different depths because the relative importance of temperature and food varies for ontogenetic stages (physiological hypothesis). We used large indoor mesocosms (Plankton Towers) to test these hypotheses experimentally.3. Temperature was the strongest factor governing the distribution, with larger proportions of the population dwelling in the food‐rich hypolimnion if the temperature gradient was shallow. There were small but significant differences between ontogenetic stages during the day, but not at night. This suggested the existence of a ‘residual’ effect of light on depth distribution in the absence of a fish cue.4. Although large individuals exhibited greater amplitude of DVM, the physiological hypothesis had to be rejected. A stage‐specific physiological effect is unlikely to be directly triggered by light, hence vertical movement of the individuals should not be synchronised. Rather, being forced into deeper layers by the residual light response during the day, large and egg‐bearing females experience a lower average temperature during day than juveniles. They probably compensate for this by spending longer time periods in warm waters at night.

Developmental responses to predation risk in morphologically defended mayflies.

Densities and species composition of predators could affect morphological defences, larval development and the timing of emergence of their prey. To address this issue we studied the morphology and life history of an ephemerellid mayfly, Ephemerella invaria, from two streams in a deciduous forested drainage basin in central New York. Both streams contained predatory fish, but densities and species composition of fish differed. A field survey provided evidence that Ephemerella inhabiting a stream with > or =10 fish species and high relative densities of fish emerged several weeks earlier and at smaller sizes than Ephemerella inhabiting a nearby tributary with approximately 2 fish species and low relative densities of fish. However, the two populations of mayflies showed no differences in defensive morphology or growth rates. In laboratory rearing experiments, we exposed Ephemerella larvae from these two locations to fish chemical cues or control water (no fish) over 2 months to test whether differences in life histories could be attributed to fish. Fish cues induced faster larval development, but also smaller size of mature Ephemerella individuals from both high and low predator locations. Although shorter development times in more dangerous environments could increase larval survival, smaller size of females results in a fecundity cost associated with this life history shift. Consistent with the field studies, laboratory rearing experiments revealed no effects of fish cues on Ephemerella's morphological defences. These data suggest that variation in the density or species composition of predators may favour the evolution of developmental plasticity to reduce mortality in the larval environment.

True and false threatening visual cues in some Mediterranean fish

Mediterranean fish of the Trachinidae and Uranoscopidae families are characterized by a poison apparatus on the 1st dorsal fin. These fish hide by burying themselves in the sand using cryptic mimicry. Nevertheless, if they are discovered before they have completely buried themselves, or perceive a potential source of danger when already covered, they will raise their 1st dorsal fin which has a bright black spot on the inter-radial membrane. We have shown that this black vexillum acts as a threatening visual cue and that the movements accompanying black mark display can be defined as aggressive mimicry. We therefore thought it interesting to investigate the black mark display in some species of Soleidae, a behaviour never before reported in the literature. In these fish, the black marks are situated on the right pectoral fin which, as a result of the distortion and re-arrangement of some anatomical parts during development, shifts to a dorsal position in adults. Soles also bury themselves in the sand, and they too display their marked fins on the approach of a possible predator, just like fish belonging to the above dangerous families.

Tadpoles' responses to risk of fish introduction.

The introduction of predatory species, such as fish, in amphibian breeding sites is one of the many likely causes of amphibian population decline. The existence of inducible or constitutive (permanent) defences is expected to temper the lethal effects of fish on tadpoles. According to current theories on the evolution of phenotypic plasticity, the amphibian species that occur in habitats that are mostly or often fish-free were expected to display inducible defences, while the species that reproduce mainly in fish ponds ought to present constitutive defences. The tested species were Rana dalmatina, Hyla arborea and R. ridibunda, respectively. As expected, R. ridibunda tadpoles were less vulnerable to fish predation than the other species. Nevertheless, all three species exhibited morphological responses in the presence of fish. Their increases in tail area and decreases in body depth were similar. However, behaviour was only modified in R. dalmatina, which exhibited lower activity rates and higher refuge use in the presence of fish cues. Such lower activity rates were related to lower growth and developmental rates. While not detected in this experiment, the existence of inducible defences in the three species suggests the existence of costs of anti-predator defence. Those costs may have delayed effects so that increasing the frequency of fish ponds may exacerbate the impact of delayed costs whatever the species, suggesting that the dynamics of species that are not fish-adverse could also suffer from the introduction of fish.

The influence of predatory fish on mayfly drift: extrapolating from experiments to nature

1. A knowledge of how individual behaviour affects populations in nature is needed to understand many ecologically important processes, such as the dispersal of larval insects in streams. The influence of chemical cues from drift‐feeding fish on the drift dispersal of mayflies has been documented in small experimental channels (i.e. < 3 m), but their influence on dispersal in natural systems (e.g. 30 m stream reaches) is unclear.2. Using surveys in 10 Rocky Mountain streams in Western Colorado we examined whether the effects of predatory brook trout (Salvelinus fontinalis) on mayfly drift, that were apparent in stream‐side channels, could also be detected in natural streams.3. In channel experiments, the drift of Baetis bicaudatus (Baetidae) was more responsive to variation in the concentration of chemical cues from brook trout than that of another mayfly, Epeorus deceptivus (Heptageniidae). The rate of brook trout predation on drifting mayflies of both species in a 2‐m long observation tank was higher during the day (60–75%) but still measurable at night (5–10%). Epeorus individuals released into the water column were more vulnerable to trout predation by both day and night than were Baetis larvae treated similarly.4. Drift of all mayfly taxa in five fishless streams was aperiodic, whereas their drift was nocturnal in five trout streams. The propensity of mayflies to drift was decreased during the day and increased during the night in trout streams compared with fishless streams. In contrast to the channel experiments, fish biomass and density did not alter the nocturnal nature nor magnitude of mayfly drift in natural streams.5. In combination, these results indicate that mayflies respond to subtle differences in concentration of fish cues in experimental channels. However, temporal and spatial variation in fish cues available to mayflies in natural streams may have obscured our ability to detect responses at larger scales.

INDUCED MORPHOLOGICAL DEFENSES IN THE WILD: PREDATOR EFFECTS ON A MAYFLY, DRUNELLA COLORADENSIS

Phenotypic plasticity may enable organisms to optimize their phenotypes in environments that are heterogeneous over time or space. For example, inducible defenses are favored for prey populations faced with variable predation risk. We studied the impact of brook trout (Salvelinus fontinalis) on the development of defensive morphological characters in larvae of the mayfly, Drunella coloradensis, both in natural streams and in a series of experiments carried out in streamside, circular, flow-through chambers. Drunella larvae in natural streams with trout had longer caudal filaments per unit body size and relatively heavier exoskeletons than Drunella in fishless streams. Female larvae that developed in fish streams were also significantly smaller and less fecund at metamorphosis than those living in fishless streams, suggesting a possible fitness cost associated with development of morphological defenses. However, timing of metamorphosis of Drunella larvae to the adult stage did not differ between fish and fishless streams. Larvae originating from fish and fishless streams were reared and exposed to water with fish cues or fishless control water for three weeks (1998) or until they developed black wing pads, i.e., just before emergence (1999). In both experiments waterborne fish cues induced the development of relatively longer caudal filaments, but only in Drunella originating from sites without fish. Waterborne fish cues had no effect on Drunella growth rates, behavior, or size at emergence. Drunella originating from fish streams had significantly lower mortality when exposed to predation by trout than Drunella originating from fishless streams. Caudal filament length appears to enhance survival, as Drunella with intact caudal filaments had lower predation rates than Drunella with their tails artificially shortened. This study provides evidence of chemically induced morphological plasticity that could reduce predation rates of these mayflies in natural stream environments.

FOOD THRESHOLD FOR DIAPAUSE INDAPHNIAUNDER THE THREAT OF FISH PREDATION

The chances of prey to survive and leave viable offspring may be determined by many environmental constraints, of which food conditions may be of key importance. When food is not limited, the high reproductive effort of a well-fed prey individual displaying various defensive responses may assure successful reproduction, whereas low food supplies may prevent it by limiting energy gains and expenditures on defense and procreation. Under low chances for survival of active forms in a local environment, production of diapausing forms of enhanced resistance to unfavorable conditions or dispersion to more favorable places may assure persistence. The laboratory batch-cultured experiments detailed here sought to test whether food concentration may influence probability of producing resting eggs by Daphnia when under chemically simulated fish predation pressure. In “fish-free” conditions, no production of resting eggs was observed with either the tested low (0.4 mg C/L) or high (1.6 mg C/L) food concentrations, whereas in “fish” treatments, resting eggs were produced by various proportions of females according to food concentration. With the limited food (0.4 mg C/L) there was production of ephippial (dormant) eggs in the early broods of almost all females in the “fish” treatment. Where food concentrations were higher, proportions of ephippial females were progressively lower, with females postponing the formation of resting eggs until later broods. At the highest food concentration (1.6 mg C/L), only about 17% of females produced ephippia when exposed to fish cues. These results are considered to indicate an adaptive response of prey individuals to a simulated danger of predation in various food conditions, determining relative gains of producing active vs. dormant offspring. It seems that D. magna may “assess” their chances of survival and successful reproduction in accordance with the anticipated danger of predation and food conditions, and enter diapause when the expected gains from diapause exceed those of active life. A graphical model explaining observed production of active vs. dormant offspring by D. magna under predation pressure at various food concentration is proposed.

Effects of fish chemical cues on the interactions between tadpoles and crayfish

We studied the effects of predatory crayfish (Pacifastacus leniusculus), the non‐lethal effects of fish chemical cues (Oncorhynchus mykiss), and the combined effects of crayfish and fish chemical cues on the performance of tadpoles of two co‐existing anuran species, Rana temporaria and Bufo bufo, in experimental pools. We also examined grazing effects on periphyton, the main food source for the tadpoles. Crayfish significantly reduced tadpole survival, particularly by feeding on Bufo. Rana benefited from reduced numbers of competitors, resulting from crayfish predation, by increased growth rate, whereas the growth rate of Bufo was unaffected by crayfish. The proportion of Rana in refuges (in relation to the number of survivors at the end of the experiment) was unaffected by crayfish, whereas proportionally more Bufo stayed in refuges in the presence of crayfish, relative to controls. Fish cues had no effect on tadpole survival of either species. During the entire larval period, Rana responded to fish cues by increasing the use of refuges relative to controls, whereas Bufo did not show any significant behavioural response to fish cues. In accordance with these observations, the proportion of Rana in refuges at the end of the experiment was high in the presence of fish cues, whereas the use of refuges by Bufo was not affected by fish cues. Predatory crayfish and fish chemical cues had additive effects on tadpole survival, growth and refuge use. Tadpoles in all treatments reduced periphyton biomass. Both crayfish and fish cues had positive indirect effects on periphyton biomass. The positive indirect effect of fish cues on periphyton was likely an effect of reduced grazing from Rana. Thus lethal, as well as non‐lethal, predator effects on prey populations can influence lower trophic levels.

Influence of predator and dietary chemical cues on the behaviour and shredding efficiency of Gammarus pulex

In two laboratory experiments, we examined short- and long-term responses of the detritivorous amphipod Gammarus pulex to chemical cues from potential predators fed various diets. In the first experiment we studied the short-term effect on G. pulex (locomotory activity) when exposed to chemical cues from three co-existing predators; sculpin (Cottus gobio), trout (Salmo trutta), and signal crayfish (Pacifastacus leniusculus). Chemicals from sculpins and trout induced a short-term decrease in locomotory activity in G. pulex, whereas crayfish did not. There was no difference in activity between G. pulex exposed to water scented by trout or sculpin, and these responses were independent of predator diet (G. pulex, Asellus aquaticus and starved). In the second experiment we examined whether longer-term exposure (4 week) to chemical cues from sculpins affects rates of leaf processing by G. pulex. During the first week, G. pulex consumed significantly more leaves in the control (i.e., no fish cue) than in the fish cue treatment. After 4 weeks, however, there was no difference in total leaf processing rate between treatments indicating an adaptation to the cue.

Behavioural response of plant-associated Eurycercus lamellatus (Ö.F. Müller) to different food sources and fish cues

The habitat preference and activity pattern of a large-bodied plant-associated chydorid, Eurycercus lamellatus, were experimentally tested under laboratory conditions using different food sources and fish cues. In the absence of epiphyton, we found significantly higher densities of E. lamellatus on plants when concentrations of phytoplankton were high, while no differences were found for real plants hosting epiphytes. In the absence of predator cues, E. lamellatus preferred plants. Exposure of E. lamellatus to chemical cues released by 0+ roach (Rutilis rutilis) previously fed on E. lamellatus or Ceriodaphnia spp. induced a habitat shift from plants to the bottom of the experimental chambers or to the sediment. However, the activity level of the test animals significantly varied between treatments. Test animals were found to be more agitated (as measured by intensity of crawling and jumping activities) in the presence of cues from E. lamellatus-fed roach then when exposed to Ceriodaphnia spp-fed roach. Most likely, the presence of cues from the conspecific E. lamellatus induced the agitated behaviour of E. lamellatus, which may be an attempt to bury within the sediment to avoid predation. Time series experiments in the presence and absence of sediment showed an almost immediate response of E. lamellatus to the addition of fish cues. The animals, however, returned to the plants during the next 7–24 h, most likely reflecting a rapid degradation of the chemical cues. The results suggest a significant influence of chemical cues on the behaviour of plant-associated microcrustaceans in the littoral zones of lakes.

Discrimination of pheromonal cues in fish: emerging parallels with insects

Many fish species employ hormonal products as sex pheromones, and these cues are often mixtures that are released with a temporal pattern. This behavior is strikingly similar to that of insects, as moths use precise blends of odorants as sex pheromones and are skillful at tracking them in spite of changes in odor intensity associated with aerial dispersal. New studies in both groups of animals suggest many parallels in the functional anatomy of olfactory pathways and the organization of information-coding circuits.

Predators can induce swarming behaviour and locomotory responses in Daphnia

1. Exposure to chemical cues released by fish induced a tendency to form and maintain aggregations in two Daphnia clones originating from habitats inhabited by fish (and invertebrate predators), while Daphnia from a clone originating from a fishless habitat did not aggregate in response to fish cues.2. Daphnia from one of the two clones responsive to fish cues, also aggregated in response to chemical cues released by invertebrate predators or to a substance released from homogenized Daphnia.3. Chemical cues released by predators and the substance released from homogenized conspecifics induced a significant decrease in Daphnia’s swimming speed and an increased readiness to perform a somersaulting escape behaviour, especially in response to light cues.

Fishless-stream mayflies express behavioural flexibility in response to predatory fish

The fish avoidance behaviour of nymphs of the grazing mayfly Baetis rhodani(Ephemeroptera) was examined. The nymphs originated from a fishless stream. To study their responses to the addition of predator cues, nymphs were exposed to (1) chemical cues from a caged fish, or (2) a freely moving diurnal fish (European minnow, Phoxinus phoxinus). The nymphs immediately increased their refuge use when exposed to a live fish, whereas chemical cues alone did not cause any avoidance responses. In a second experiment, the effects of (1) fish chemicals and (2) a fish model plus fish chemicals on the diel refuge use patterns of Baetisnymphs were examined. In the presence of a fish model, more nymphs were outside the refuges during the first few hours of darkness, when fish predators are not active, than at any other time of day. A similar but non-significant trend was observed when only chemical cues of fish were present, whereas refuge use in the control treatment was aperiodic. Baetisnymphs were thus able to assess the fish predation risk and to respond by quickly adjustable, flexible avoidance behaviour. Spatial and temporal variation in predation risk, and adult dispersal between fishless and fish-inhabited streams, may be the key factors promoting the maintenance of flexible fish avoidance behaviour in stream-dwelling mayfly nymphs.

Daphnia Behaviour as a Bioassay of Fish Presence or Predation

1. Fish cues are associated with changes in Daphnia behaviour, however, the causes of these responses are generally unknown. 2. Two kinds of experiments were done in order to test whether the predator cue inducing changes in Daphnia galeata mendotae was : in solution and molecular ; whether the cue came from fish or from other Daphnia ; whether the presence of fish was sufficient to generate the cue ; whether a predator had to be eating and digesting prey ; if the type of food was important. 3. Results of the two experiments indicated that : the cue was molecular. It was only generated by fish digesting live food, unlike bioassay experiments on Daphnia magna. It did not require that naive Daphnia were pre-conditioned. There was between-clone variation for responses to water conditioned by fish feeding on commercial worms, whereas all the clones tested in these experiments responded strongly to fish feeding on Daphnia. 4. Between-genotype variation for specificity and sensitivity to chemical cues suggests the potential for different Daphnia species in different habitats to evolve disparate responses to the same kind of predator.

Effects of visual, chemical and tactile cues of fish on the behavioural responses of tadpoles

Abstract. The anti-predator behaviour of two closely related species of tadpoles, Rana lessonae and Rana esculenta, was examined in response to tactile, visual and chemical cues of a fish predator, pike Esox lucius, alone and in all combinations. Tadpoles were hatched and reared in the laboratory to eliminate any experience from natural habitats. The chemical cue decreased swimming and increased the use of areas of the test chambers furthest away from the fish significantly more than tactile or visual cues. The combination of chemical and tactile cues yielded the strongest responses for swimming, resting and use of the edges of the test chambers, while responses to the tactile cue alone did not differ significantly from the control treatment. It is suggested that the tactile cues used, simulating the movement of water by a fish, give tadpoles additional information about the location and the distance of the predator that is not present in chemical cues alone. The visual cue alone or in combination with the tactile cue produced weak responses that did not differ from the control treatment. It may be that tadpoles have poor vision or that visual cues may not be reliable in benthic aquatic habitats with limited view caused by vegetation, suspended sediments, or phytoplankton. The two species responded differently: R. lessonae used the refuge significantly more than did R. esculenta; conversely R. esculenta used the open water significantly more than did R. lessonae. The lack of significant species by treatment interactions indicates that these responses do not reflect differential behaviour towards predator cues, but rather are inherent species differences.

Behavioral mechanisms controlling vertical migration in Daphnia

We used infrared video monitoring to study cladoceran vertical migration in laboratory tanks exposed to natural and simulated daylight cycles. There are changes in the behavior patterns at different times of the year, with both Daphnia magna and Daphnia longispina showing increased vertical migration and greater average depth later in the year. This change in behavior pattern is due to temperature, not daylength, changes. Our animals show a complex endogenous migration pattern, with a strong downward excursion in the middle of the night, another before dawn, and then a morning rise, of which only the last depends on a visual stimulus. We propose that the morning rise acts as a correcting movement bringing animals to a depth just safe from visual predators. The midnight sinking is unlikely to be due to a random spreading‐out process. Fish taste cues enhanced the dawn excursion, but not the midnight one. Responses to fish cues were most pronounced for D. magna at low temperatures.

17 alpha,20 beta-dihydroxy-4-pregnen-3-one 20-sulphate is a potent odorant in precocious male Atlantic salmon (Salmo salar L.) parr which have been pre-exposed to the urine of ovulated females.

Electrophysiological recordings from the olfactory epithelium have shown that 17 alpha,20 beta-dihydroxy-4-pregnen-3-one 20-sulphate (17,20 beta-P-sulphate; a conjugate of the oocyte-maturation-inducing steroid in teleosts) is a potent odorant in precocious male Atlantic salmon (Salmo salar L.) parr. However, the olfactory epithelium of these fish only appeared to be responsive to the steroid after stimulation with the urine of ovulated female Atlantic salmon. Immature fish did not respond at any time. Stimulation with urine from immature and precocious male Atlantic salmon parr did not make the olfactory epithelium of precocious male salmon parr responsive to the steroid. 17,20 beta-P-sulphate was found in the urines of ovulated females, precocious male parr and mature male Atlantic salmon. The findings are discussed in relation to the possible role of 17,20 beta-P-sulphate in the physiology of Atlantic salmon.

The detection of certain predators via olfaction by small-mouthed salamander larvae ( Ambystoma texanum)

Larvae of the small-mouthed salamander (Ambystoma texanum) showed an increase in refuge use when exposed to chemical cues from a predaceous fish. The percentage of time spent outside of refuge was significantly reduced relative to controls when larvae were exposed to chemical cues from fish, but was not different from the controls when larvae were exposed to chemical cues from three other potential predators. A. texanum larvae responded to these chemical cues via olfaction. Larvae that had their external nares plugged with a gelatinous paste did not respond to fish cues, while sham-treated larvae showed an avoidance of fish cues.

Comment: Sexually selected infanticide among female birds

Prey may use multiple sensory channels to detect predators, whose cues may differ in altered sensory environments, such as turbid conditions. Depending on the environment, prey may use cues in an additive/complementary manner or in a compensatory manner. First, to determine whether the purely aquatic Barton Springs salamander, Eurycea sosorum, show an antipredator response to visual cues, we examined their activity when exposed to either visual cues of a predatory fish (Lepomis cyanellus) or a non-predatory fish (Etheostoma lepidum). Salamanders decreased activity in response to predator visual cues only. Then, we examined the antipredator response of these salamanders to all matched and mismatched combinations of chemical and visual cues of the same predatory and non-predatory fish in clear and low turbidity conditions. Salamanders decreased activity in response to predator chemical cues matched with predator visual cues or mismatched with non-predator visual cues. Salamanders also increased latency to first move to predator chemical cues mismatched with non-predator visual cues. Salamanders decreased activity and increased latency to first move more in clear as opposed to turbid conditions in all treatment combinations. Our results indicate that salamanders under all conditions and treatments preferentially rely on chemical cues to determine antipredator behavior, although visual cues are potentially utilized in conjunction for latency to first move. Our results also have potential conservation implications, as decreased antipredator behavior was seen in turbid conditions. These results reveal complexity of antipredator behavior in response to multiple cues under different environmental conditions, which is especially important when considering endangered species.