Visual feeding of fish in a turbid environment: Physical and behavioural aspects

Turbidity has both positive and negative effects on prey detection, by increasing or diminishing the contrast between prey and background due to the scattering of light. The positive effect of turbidity on prey contrast depends on the optical properties, scattering properties of suspended particles and the visual sensitivity of the predator.

The positive effect of turbidity is pronounced for larval fish, given that their visual field is short, leaving fewer particles between them and their prey to scatter light and interfere with detection. This relationship, together with a decreased risk of predation, makes turbid environments more optimal for some species and size groups of fish (planktivores and fish larvae) and less so for others (adult piscivore fish). Thus, turbidity might have a structuring effect on a fish community. Recently it has been demonstrated that UV light might have positive effects on prey detection and consumption. How UV light might interact with different kinds of particles producing turbidity is not well documented.     

Ultraviolet light influences habitat preferences in a fish under predation risk

Environmental light conditions are of general importance in predator–prey interactions. In aquatic systems, prey individuals experience different levels of predation risk depending on the properties of the visual environment, such as structural complexity or water transparency. To reduce the threat of predation, prey should move to habitats providing better protection against visual predators. We studied the role of UV wavelengths in habitat choice behaviour under predation risk in a fish, the three-spined stickleback (Gasterosteus aculeatus) that uses UV signals in different contexts of intraspecific communication. In a laboratory experiment sticklebacks were exposed to a predatory threat and given the choice between two escape habitats, one providing full-spectrum conditions including UV light (UV+) and one without UV wavelengths (UV−). Fish from two rearing treatments were tested, one group had been raised under natural lighting conditions (UV+), the other group under UV-deficient lighting conditions (UV−). Sticklebacks from the UV+ group preferred the UV− habitat as a refuge which suggests that predator avoidance behaviour is UV-related in this species with UV− conditions presumably being advantageous for prey fish. However, individuals from the UV− treatment group were equally attracted to both presented light habitats. It is possible that these fish could not discriminate between the two light habitats due to physiological limitations caused by their rearing conditions. Further control trials with neutral-density filters revealed that the UV− habitat preference of UV+ fish in the main experiment was rather not influenced by a difference in achromatic brightness between the UV+ and UV− habitat.     

The UV visual world of fishes: a review

Ultraviolet-A radiation (320–400 nm) is scattered rapidly in water. Despite this fact, UV is present in biologically useful amounts to at least 100 m deep in clear aquatic environments. Discovery of UV visual pigments with peak absorption at around 360 nm in teleost cone photoreceptors indicates that many teleost fishes may be adapted for vision in the UV range. Considering the characteristic absorption curve for visual pigments, about 18% of the downwelling light that illuminates objects at 30-m depth would be available to UV-sensitive cones. Strong scattering of UV radiation should produce unique imaging conditions as a very bright UV background in the horizontal view and a marked veiling effect that, with distance, obscures an image. Many teleosts have three, or even four, classes of cone cells mediating colour vision in their retina and one can be sensitive to UV. These UV-sensitive cones contain a visual pigment based on a unique opsin which is highly conserved between fish species. Several powerful methods exist for demonstration of UV vision, but all are rather demanding in terms of technique and equipment. Demonstration that the eye lacks UV-blocking compounds that are present in many fish eyes is a simpler method that can indicate the possibility of UV vision. The only experimental evidence for the use of UV vision by fishes is connected to planktivory: detection of UV-opaque objects at close range against a bright UV background is enhanced by the physical properties of UV light. Once present, perhaps for the function of detecting food, UV vision may well be co-opted through natural selection for other functions. Recent discovery that UV vision is critically important for mate choice in some birds and lizards is a strong object lesson for fish ecologists and behaviourists. Other possible functions amount to far more than merely adding a fourth dimension to the visible spectrum. Since UV is scattered so effectively in water, it may be useful for social signalling at short range and reduce the possibility of detection by other, illegitimate, receivers. Since humans are blind to UV light, we may be significantly in error, in many cases, in our attempts to understand and evaluate visual aspects of fish behaviour. A survey of the reflectance properties of skin pigments in fishes reveals a rich array of pigments with reflectance peaks in the UV. For example, the same yellow to our eyes may comprise two perceptually different colours to fish, yellow and UV-yellow. It is clearly necessary for us to anticipate that many fishes may have some form of UV vision.     

How Much Does Ultraviolet Radiation Contribute to the Feeding Performance of Rainbow Trout, Oncorhynchus mykiss, Juveniles under Natural Illumination?

Most research on environmental effects of ultraviolet radiation (UVR) has focused on its potential negative consequences. However, natural UVR can also be beneficial to living organisms (e.g., vitamin D synthesis, UV vision, germicide activity). UV vision has been demonstrated in a variety of animals including several invertebrates and vertebrates. Juvenile rainbow trout, Oncorhynchus mykiss, has a retinal photoreceptor, which is sensitive to UVR between 360 and 370 nm. Among other functions, UV vision has been proposed to contribute to prey detection by enhancing the contrast between the prey and its background. We performed a series of feeding experiments with juvenile rainbow trout and several zooplankters as prey. The fish were allowed to feed either under full solar radiation, or under solar radiation from which the UV component had been removed using a long-pass cut off filter. We found that the removal of UV wavelengths had no effect on the number of prey eaten or on the preference for particular food items. This is contrary to published studies reporting prey detection enhancement mediated by UV vision in rainbow trout. This disparity in the results may be due to our use of natural radiation instead of artificial UV sources, in which the visible component is poorly represented. Although our results do not disproof the presence of UV vision in juvenile rainbow trout, they do cast doubts about its significance in enhancing feeding performance in a natural light environment.     

To fear or to feed: the effects of turbidity on perception of risk by a marine fish

Coral reefs are currently experiencing a number of worsening anthropogenic stressors, with nearshore reefs suffering from increasing sedimentation because of growing human populations and development in coastal regions. In habitats where vision and olfaction serve as the primary sources of information, reduced visual input from suspended sediment may lead to significant alterations in prey fish behaviour. Here, we test whether prey compensate for reduced visual information by increasing their antipredator responses to chemically mediated risk cues in turbid conditions. Experiments with the spiny damselfish, Acanthochromis polyacanthus, found that baseline activity levels were reduced by 23 per cent in high turbidity conditions relative to low turbidity conditions. Furthermore, risk cues elicited strong antipredator responses at all turbidity levels; the strongest antipredator responses were observed in high turbidity conditions, with fish reducing their foraging by almost 40 per cent, as compared with 17 per cent for fish in clear conditions. This provides unambiguous evidence of sensory compensation in a predation context for a tropical marine fish, and suggests that prey fish may be able to behaviourally offset some of the fitness reductions resulting from anthropogenic sedimentation of their habitats.     

Visual Detection of Speckles in the Fish Xenotoca variata by the Predatory Snake Thamnophis melanogaster in Water of Different Turbidity

Semi-aquatic snakes integrate visual and chemical stimuli, and prey detection and capture success are therefore linked to the display of visual predatory behavior. The snake Thamnophis melanogaster responds preferentially to individuals of the fish Xenotoca variata with a greater number of bright, colorful spots (lateral speckles) compared with those with a smaller number; however, water turbidity can reduce underwater visibility and effect the vulnerability of fish. In this study, we tested whether the presence of iridescent speckles on the flanks of male X. variata interacted with water turbidity to modify the predatory behavior displayed by the snake T. melanogaster. We predicted that in an experimental laboratory test, the snakes would increase the frequency of their predatory behavior to the extent that the water turbidity decreases. The snakes were tested at six different levels of water turbidity, in combination with three categories of male fish (with few, a median number of, or many speckles). The results showed that in a pool with high or zero turbidity, the number of speckles is not a determining factor in the deployment of the predatory behavior of the snake T. melanogaster toward X. variata. Our findings suggest that snakes can view the fish at intermediate percentages of turbidity, but the number of speckles in male X. variata is irrelevant as an interspecific visual signal in environments with insufficient luminosity. The successful capture of aquatic prey is influenced by integration between chemical and visual signals, according to environmental factors that may influence the recognition of individual traits.     

Turbidity amplifies the non‐lethal effects of predation and affects the foraging success of characid fish shoals

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Predator–prey encounter rates in freshwater piscivores: effects of prey density and water transparency

One of the most fundamental components of predator–prey models is encounter rate, modelled as the product of prey density and search efficiency. Encounter rates have, however, rarely been measured in empirical studies. In this study, we used a video system approach to estimate how encounter rates between piscivorous fish that use a sit-and-wait foraging strategy and their prey depend on prey density and environmental factors such as turbidity. We first manipulated prey density in a controlled pool and field enclosure experiments where environmental factors were held constant. In a correlative study of 15 freshwater lakes we then estimated encounter rates in natural habitats and related the results to both prey fish density and environmental factors. We found the expected positive dependence of individual encounter rates on prey density in our pool and enclosure experiments, whereas the relation between school encounter rate and prey density was less clear. In the field survey, encounter rates did not correlate with prey density but instead correlated positively with water transparency. Water transparency decreases with increasing prey density along the productivity gradient and will reduce prey detection distance and thus predator search efficiency. Therefore, visual predator–prey encounter rates do not increase, and may even decrease, with increasing productivity despite increasing prey densities.     

Non-additive effects of macrophyte cover and turbidity on predator–prey interactions involving an invertivorous fish and different prey types

Habitat complexity, turbidity and prey type availability affect trophic dynamics, and an improved understanding of how these three factors work together could facilitate interpretations of trophic dynamics in environments with regime shifts. We conducted an experiment to cross these three factors, hypothesising that increasing both turbidity and macrophyte cover reduce consumption of Chironomids more than they reduce consumption of Cypridids. Our results did not support our hypothesis, suggesting that the effect of macrophyte cover on predation depends on turbidity. However, the magnitude of this combined effect is the same as that of turbidity alone. Moreover, turbidity affected predation on both prey types similarly. In addition, the effect of macrophyte cover on predation also depended on prey type. We argue that visual and physical refuges may be as effective as shelter, but macrophyte cover may benefit smaller prey items. This may lead to higher predation rates by small-sized fish on invertebrates during periods of low turbidity devoid of macrophyte cover and to similar predation rates on invertebrates during periods of low turbidity and abundant macrophytes, high turbidity and scarce macrophytes or high turbidity and abundant macrophyte cover.     

Chromaticity in the UV/blue range facilitates the search for achromatically background-matching prey in birds

A large variety of predatory species rely on their visual abilities to locate their prey. However, the search for prey may be hampered by prey camouflage. The most prominent example of concealing coloration is background-matching prey coloration characterized by a strong visual resemblance of prey to the background. Even though this principle of camouflage was recognized to efficiently work in predator avoidance a long time ago, the underlying mechanisms are not very well known. In this study, we assessed whether blue tits (Cyanistes caeruleus) use chromatic cues in the search for prey. We used two prey types that were achromatically identical but differed in chromatic properties in the UV/blue range and presented them on two achromatically identical backgrounds. The backgrounds had either the same chromatic properties as the prey items (matching combination) or differed in their chromatic properties (mismatching combination). Our results show that birds use chromatic cues in the search for mismatching prey, whereupon chromatic contrast leads to a ‘pop-out’ of the prey item from the background. When prey was presented on a matching background, search times were significantly higher. Interestingly, search for more chromatic prey on the matching background was easier than search for less chromatic prey on the matching background. Our results indicate that birds use both achromatic and chromatic cues when searching for prey, and that the combination of both cues might be helpful in the search task.     

Opsin switch reveals function of the ultraviolet cone in fish foraging

Although several studies have shown that ultraviolet (UV) wavelengths are important in naturally occurring, visually guided behaviours of vertebrates, the function of the UV cone in such behaviours is unknown. Here, I used thyroid hormone to transform the UV cones of young rainbow trout into blue cones, a phenomenon that occurs naturally as the animal grows, to test whether the resulting loss of UV sensitivity affected the animal''s foraging performance on Daphnia magna, a prey zooplankton. The distances and angles at which prey were located (variables that are known indicators of foraging performance) were significantly reduced for UV knock-out fish compared with controls. Optical measurements and photon-catch calculations revealed that the contrast of Daphnia was greater when perceived by the visual system of control versus that of thyroid-hormone-treated fish, demonstrating that the UV cone enhanced the foraging performance of young rainbow trout. Because most juvenile fishes have UV cones and feed on zooplankton, this finding has wide implications for understanding the visual ecology of fishes. The enhanced target contrast provided by UV cones could be used by other vertebrates in various behaviours, including foraging, mate selection and communication.     

Red fluorescence increases with depth in reef fishes,supporting a visual function,not UV protection

Why do some marine fishes exhibit striking patterns of natural red fluorescence? In this study, we contrast two non-exclusive hypotheses: (i) that UV absorption by fluorescent pigments offers significant photoprotection in shallow water, where UV irradiance is strongest; and (ii) that red fluorescence enhances visual contrast at depths below −10 m, where most light in the ‘red’ 600–700 nm range has been absorbed. Whereas the photoprotection hypothesis predicts fluorescence to be stronger near the surface and weaker in deeper water, the visual contrast hypothesis predicts the opposite. We used fluorometry to measure red fluorescence brightness in vivo in individuals belonging to eight common small reef fish species with conspicuously red fluorescent eyes. Fluorescence was significantly brighter in specimens from the −20 m sites than in those from −5 m sites in six out of eight species. No difference was found in the remaining two. Our results support the visual contrast hypothesis. We discuss the possible roles fluorescence may play in fish visual ecology and highlight the possibility that fluorescent light emission from the eyes in particular may be used to detect cryptic prey.     

The effects of turbidity and vegetation on the risk of juvenile salmonids, Oncorhynchus spp., to predation by adult cutthroat trout, O. clarkii

Synopsis During their seaward migration, juvenile salmonids encounter structural and visual cover which varies between and within watersheds. In this study, the effects of two types of cover (turbidity and artificial vegetation) on the predation mortality of juvenile salmonids exposed to fish piscivores was investigated in outdoor concrete ponds. During experiments, adult coastal cutthroat trout, Oncorhynchus clarkii clarkii, were allowed to feed on juvenile salmonid prey — chinook salmon, O. tshawytscha, chum salmon, O. keta, sockeye salmon, O. nerka, and cutthroat trout — in separate trials. Daily instantaneous per capita predation rate was determined for each turbidity and vegetation treatment, within each trial. Mean predation rates varied between 1% and 76% daily. In the presence of cover, mean daily predation rates were 10–75% lower than those in controls (no vegetation and clear water), depending on prey species. Predation rates were significantly lower in the presence of vegetation cover and did not covary with prey size or species. The effects of turbidity were generally not significant and were not additive with the effects of vegetation. However, turbidity appeared to significantly reduce the effectiveness of vegetation as cover for juvenile chinook and sockeye salmon. We suggest that these two forms of cover do not affect risk of predation by fish piscivores to juvenile salmonids via the same mechanism.     

The effects of turbidity on prey consumption and selection of zooplanktivorous Gasterosteus aculeatus L.

It is well documented that reduced visibility caused by elevated turbidity can affect feeding of fish, yet the extent to which selective zooplanktivory is altered in turbid conditions remains ambiguous. In this study, we examined the influence of natural sediment-induced turbidity on the overall prey consumption and selective predation of a common brackish water littoral zooplanktivore, the particulate feeding three-spined stickleback (Gasterosteus aculeatus L.). We hypothesized that the effects of turbidity on prey consumption and prey type selection would be pronounced due to the vision-oriented feeding of this species and that these effects would differ between genders. Using aquarium experiments with three different groups of cladocerans and copepods varying in size and behavior, we studied prey consumption and selectivity of this key planktivore in varying turbidity treatments. Our results indicated significantly decreased total prey consumption in the high turbidity treatments, as well as altered selective feeding on copepods and an enhanced preference for larger cladocerans. We found gender-dependent differences in prey consumption, which are consistent with observations of other visually feeding fish with sexual size dimorphism. We conclude that high turbidity, such as that occurring in shallow coastal areas, may affect selective feeding in vision-oriented zooplanktivores and that these effects may be gender-related.     

Physiological and visual refuges in a metalimnion: an experimental study of effects of clay turbidity and an oxygen minimum on fish predation

1. The effectivity of elevated clay turbidity and low-oxygen concentration in the metalimnion as refuges for chaoborid larvae against fish predation was studied in experimental water columns.
2. When 70–80 nephelometric turbidity unit clay turbidity was combined with 3–4 mg L⁻¹ oxygen concentration, prey capture rate by fish (golden orfe Leuciscus idus ) was reduced by 74% compared with the control treatment with no refuges. Oxygen and turbidity refuges alone did not significantly reduce the feeding rate.
3. All fish in the control treatment dwelled in the metalimnion, but 36% of the fish in the low-oxygen treatment and 23% of the fish in the turbidity treatment stayed in the epilimnion. In the combined treatment, 54% of the fish were in the epilimnion.
4. The results demonstrated that a combination of moderately elevated turbidity and lowered oxygen concentration in the metalimnion is an effective protection against fish predation, while turbidity or oxygen refuge alone are much less effective.
5. In the treatment with the combined refuge, oxygen concentration limited the time fish could spend in the metalimnion and turbidity affected the detection of prey through changes in reactive distance.
6. Because of the combined effects of turbidity and oxygen refuges, planktivorous fish and phantom midge larvae may co-occur in clay-turbid lakes in high densities. Such situation is problematic for biomanipulation, which aims to enhance the grazing rate of zooplankton through reduction of planktivorous fish.     

Altered visual environment affects a tropical freshwater fish assemblage through impacts on predator–prey interactions

1. Increased turbidity and siltation caused by rock quarrying, mining, and deforestation are pervasive disturbances in aquatic systems. Turbidity interferes with vision for aquatic organisms, potentially altering predator–prey interactions.
2. We studied the effects of these disturbances in Trinidadian streams by surveying predators and their shared prey both in streams with versus without quarries as well as in a focal stream before and after the establishment of a quarry. Then, to evaluate whether differential foraging success in turbid water might underlie abundance patterns of predators, we experimentally induced turbidity in mesocosms and measured predator foraging success.
3. Upstream quarry presence had a dramatic effect on the benthic structure of streams, greatly increasing siltation. A substantial decrease in the abundance of a diurnal cichlid predator (Crenicichla frenata) was associated with quarry presence, while a nocturnal erytherinid predator (Hoplias malabaricus) was equally as abundant in streams with or without quarries. The density of their shared prey, the Trinidadian guppy (Poecilia reticulata) remained unchanged.
4. In mesocosm trials, Crenicichla were less successful predators with turbidity, whereas Hoplias performed equally across turbidities. These foraging success results help explain differences in demographic shifts in response to turbidity for both predators.
5. By relating short-term effects of an anthropogenically altered visual environment on species interactions to abundance patterns of predators and prey, this study helps to identify an important mechanism whereby changes to species’ visual ecology may have long-term effects on population biology.

     

Characteristics of reaction field and the reactive distance of a planktivore, Pseudorasbora parva (Cyprinidae), in various environmental conditions

The characteristics of the reaction field and the reactive distance of the Stone moroko (Pseudorasbora parva) were studied under three environmental conditions (structural complexity, light intensity and turbidity) and three prey sizes. In optimal experimental conditions, under no structural complexity, light intensity of 200 lux and turbidity less than 1 NTU (Nephelometric Turbidity Units), the cross-section of the reaction field was found to be elliptic with a bearing angle larger than the elevation angle, but both angles changed slightly depending on environmental conditions. The reactive distance was large, and the fish frequently attacked prey that was located within 15–60 degrees to each side from the frontal direction of a fish (i.e., ± 15 degrees from the axis of the fish body) horizontally. In the light intensity below 50 lux or turbidity above 10 NTU, however, the attack frequency and the reactive distance in the frontal direction of a fish did not differ from other horizontal directions in the reaction field. The average reactive distance increased proportionally with increasing strand distance, but it gradually reached a constant value for strand distances greater than about 3.6 times the fish body length. The average reactive distance increased in the light intensity range of 10–200 lux and decreased negatively with turbidity increasing. The average reactive distance increased with larger prey size, but the rate of increase of the reactive distance gradually decreased.     

Ultraviolet vision and foraging in dip and plunge diving birds

Many fishes are sensitive to ultraviolet (UV) light and display UV markings during courtship. As UV scatters more than longer wavelengths of light, these signals are only effective at short distances, reducing the risk of detection by swimming predators. Such underwater scattering will be insignificant for dip and plunge diving birds, which prey on fishes just below the water surface. One could therefore expect to find adaptations in the eyes of dip and plunge diving birds that tune colour reception to UV signals. We used a molecular method to survey the colour vision tuning of five families of dip or plunge divers and compared the results with those from sister taxa of other foraging methods. We found evidence of extended UV vision only in gulls (Laridae). Based on available evidence, it is more probable that this trait is associated with their terrestrial foraging habits rather than piscivory.     

The role of vision in the predatory behaviour of natricine snakes

Early workers concluded that ingestively naive garter snakes (Thamnophis) recognize chemical cues from their normal prey, and that such cues are sufficient to elicit prey attack, whereas visual prey cues are not sufficient. In the light of recent observations on how garter and water snakes (Nerodia) forage, new tests were made of the role of visual stimuli in the aquatic predation of several natricine species. Both experienced and ingestively naive snakes oriented to and attacked a fish model in plain water, although they made more orientations and attacks when diffuse fish odour was present in the water. Fish odour in water also elicited increased aquatic searching behaviour. Early views on the role of vision in the predation of newborn natricine snakes require modification, and there is a need for investigation of the properties of effective visual stimuli and the ontogeny of responsiveness to them.     

Relationship of turbidity to the stages of platelet aggregation

The process of platelet aggregation as detected by turbidity changes in the platelet aggregometer was studied relative to light scattering by large particles. For latex beads a plot of light scattering intensity/unit mass versus particle size gave increased light scattering intensity for small particle sizes but decreased scattering at large particle size. This behavior is predicted by Rayleigh-Gans theory. These results were related to the platelet aggregometer, an optical instrument used to measure the association of small particles (monomeric platelets) to large particles (platelet aggregates). Formalin-fixed platelets do not show changes in light transmission due to energy-requiring processes, such as shape change, so that turbidity changes in the presence of aggregating agents could be attributed to a change in platelet aggregation state. Small platelet aggregates showed increased turbidity compared to a similar mass of monomeric platelets. In fact, very large platelet aggregates that were visible to the unaided eye were needed to produce a decrease in light scattering intensity. Thus, turbidity can either increase or decrease with platelet aggregation depending on the size of the aggregates. Studies of platelet aggregation that show no initial increase in turbidity must be characterized by dominance of large platelet aggregates and monomeric platelets.