Responses of freshwater fish to fluorescent lures at daylight

Many companies manufacture fishing lures and baits of bright fluorescent colors and position these products in the consumer markets as effective tools to attract and catch fish. However, numerous scientific, technical and applied investigations and recreational fishing practice show that these assertions are, as minimum, exaggerated.

In general case, fluorescence is an optical phenomenon when molecules of some substances absorb light in the ultraviolet or visual parts of the electromagnetic spectrum and immediately re-emit it with the longer wavelength. Because the falling light is partly reflected by these substances and the reflected light is mixed with the light of fluorescence, the eyes of human and animals (if they have color vision) perceive the total colors of these substances as “more bright”.

Spectral sensitivity

Fresh waters are optically more turbid than sea waters, so the maximum of spectral sensitivity in freshwater fish is shifted to the red part of the visual spectrum. In bluegill sunfish, Lepomis macrochirus, for example, the maximum of spectral sensitivity is shifted to 620-640 nm (orange part of the spectrum) (Hawryshyn et al., 1988). According to Kawamura & Kishimoto (2002), the maximum of spectral sensitivity in largemouth bass, Micropterus salmoides, is shifted even to 673 nm (red part of the spectrum). It means that for freshwater fish red and orange colors are brighter than other colors, in full contradiction with the perception of saltwater fish and human.

This red or orange shift of the maximum of spectral sensitivity is typical for other freshwater fish (Protasov, 1978).

Turbidity

Turbid waters decrease overall intensity of ambient light, decrease via scattering an ability of receivers to resolve silhouettes and more (for review, see Utne-Palm, 2002). In particular, turbidity affects color perception of freshwater fish, their color patterns and communication with the assistance of color signals.

For example, with an increase in turbidity of habitat males of red shiners, Cyprinella lutrensis, develop more intensive red fins (Dugas & Franssen, 2011). According to Kelley et al. (2012), rainbowfish, Melanotaenia australis, in the dissolved organic matter treatment show an increase in the area and brightness of their orange striped patterns.

More generally, turbidity weakens color signals in inter-sexual selection (Seehausen et al. 1997), even limiting species recognition in mate choice.

Fluorescent colors underwater

Overall, fluorescent colors are brighter than ordinary colors and are more visible underwater (Kinney et al., 1967). In turbid water (like Thames river), orange fluorescent color is most visible for the human’s eye than other colors.

Other animals

For fruit fly, Anastrepha suspensa, traps of orange fluorescent color are more attractive than traps of ordinary orange color (Greany et al., 1978).

Dull males versus bright males

Accustomed to think that females, in fish and other animals with the sexual dimorphism, prefer to mate with bright males than with dull males. In turn, generally recognized that bright males are more vulnerable to predation risks than dull males. However, special and most detailed investigations of these questions reveal that these “generally accepted rules” are not  universal.

For example, Breden & Stoner (1987) have shown that females of guppy, Poecilia reticulata, from high-predation populations show genetically determined, lower preference for brightly colored males than do females from areas of low predation. In turn, predatory pike cichlid, Crenicichla alta, prefer to attack in sex-mixed schools of guppy dull and most profitable females than bright and less profitable males (Pocklington & Dill, 1995).

In other words, detection of potential prey even from the longer distance and the real attack on prey need the different decisions making and are separated in time.

Transgenic fluorescent zebrafish

The development of transgenic zebrafish, Danio rerio, and other fish with green, yellow, orange, red and other fluorescent colors has opened an opportunity to study the role of fluorescence in intraspecific and interspecific relations in fish and their predators under the control conditions. Note that under the day light transgenic zebrafish have slightly more intensive colors than wildtype zebrafish (usually with the longitudinal bluish and yellowish stripes), but under the special ultraviolet illumination (invisible for human) they become extremely bright (for example, see photos given by Gong et al., 2003).

In our context, Cortemeglia & Beitinger (2006) have found that under the day light predatory largemouth bass, M. salmodes, consume red fluorescent zebrafish and wildtype zebrafish approximately in an equal proportion. According to Jha (2010), snakehead, Channa striatus, consume under the day conditions both red fluorescent zebrafish and wildtype zebrafish, but try to avoid red fluorescent zebrafish. However, Hill et al. (2011) have found that largemouth bass consume under the day conditions about two times more red fluorescent zebrafish than wildtype zebrafish and concluded that transgenic fish are more susceptible to predation.

In boreal countries (like Ukraine), wildtype and transgenic zebrafish are not survive in the nature due to the cold winters. So, in our experiments we used common perch, Perca fluviatilis, as native predators (about 5-7 cm total length) and aquarium forms of wildtype and red fluorescent zebrafish as popetial prey.

An experimental aquarium was located near the large laboratory windows and was illuminated with the ambient light, which varied from daylight to twilight and nightlight. Because perch were not familiar with both forms of zebrafish, they learnt to hunt novel prey (note, perch are diurnal and crepuscular predators). Briefly, perch passed from the first observations for prey to approaches, chases and the first prey captures (about mutual learning in predators and prey, see Lescheva & Zhuykov, 1989). Under the day and crepuscular illuminations, no preferences of perch towards wildtype or red fluorescent zebrafish (relatively dull under these illuminations) were observed. However, under additional ultraviolet illumination red fluorescent zebrafish became very bright, and perch avoided them (during 3 days of observations none of bright prey were eaten).

Fig. 1. Transgenic fluorescent danios (http://shop.glofish.com/products/glofish-danio-package).

According to our abservations, pike, Esox lucius, another diurnal and crepuscular predator, does not avoid dull red fluorescent zebrafish but avoid bright (UV illuminated) prey.

In the wild nature, visually guided fish may include in their diets new and brightly colored prey but only after long-term testing of these prey and formation of search image in respect to these prey. For example, Hope (1984) has informed that wild trout included in their diet an invasive species of beetles with bright coloration only through about month of acquaintance with this new prey and their testing.

Large fluorescent objects versus small fluorescent implants

It is necessary to distinguish large fluorescent objects and small fluorescent implants used to tag fish. It is shown (e.g., Catalano et al., 2001; Roberts & Kilpatrick, 2004) that small but bright fluorescent implants may attract predators and thus decrease the recapture rate of tagged fish in the nature.

Fluorescent fishing lines

It is shown that largemouth bass may distiguish white, yellow and green fluorescent fishing lines but only after several trials with attached worms to these lines (Miller & Janzow, 1979).

Fishing practice. Part 1

There are fish habitats that allow to confirm the attractiveness of red or orange fluorescent lures at the statistic level. These habitats are rivers with clayish banks, clay pits or clay ponds in which water may be very turbid especially under wind and after rains.

Using one of these localities, we tested soft plastic lures of red fluorescent color and ordinary red color. Lures, namely curly tails of 3 cm length, were rigged in pairs at the distance of 10-12 cm between each other. Fish could observe both lures simultaneuosly for free choice, so the sign test for paired comparisons was used for statistics.

Tests were carried out in summer in clayish locality of Goryn river (Belarus). According to visual guide, turbidity of the water was about 90 NTU (nephelometric turbidity units) and more under wind. Red fluorescent lures were illuminated naturally in the air under the sun light.

During 2 days of experiments, overall 39 fish were caught using standard spinning technique. They were adult perch, P. fluviatilis, and Donets ruffe, Gymnocephalus acerina, as well as juvenile pike, E. lucius, zander, Stizostedion lucioperca, asp, Aspius aspius, and chub, Leuciscus cephalus. Of these 39 fish, 28 fish preferred red fluorescent lures over ordinary red lures (sign test, P < 0.01).

However, in more or less clear waters red or orange fluorescent lures may seem too bright and thus they may deter or scare predatory fish.

It is known that mature males of three-spined sticklebacks, Gasterosteus aculeatus, with the red breast aggresively attack other mature males and artificial wooden red models (Darkov, 1980). According to our observations in the nature, nest guarding males of sticklebacks attack in the same manner approaching soft plastic shads (3 cm length) of ordinary red color but avoid much more conspicuous red fluorescent shads (additionally to sun light illuminated by LED lantern).

Fishing practice. Part 2

Other fish habitats suitable to use red or orange fluorescent lures are river back waters, lakes and ponds in which water is saturated with the soluble organic substances and suspensions (like algae). In these habitats, for example, some natural white maggots with one red fluorescent maggot can be more attractive for carp, Cyprinus carpio, tench, Tinca tinca, and other cyprinids than the same natural white maggots without one very visible red fluorescent maggot. However, preferences of cyprinid fish to red or orange fluorescent lures are not widespread, stable and suitable for statistic confirmations because colors of baits are not prefered stimuli for these fish.

Foraging carps and other large bentivorous fish increase turbidity of water bodies (e.g., Richardson et al., 1995; Roberts et al., 1995; Drenner et al., 1997; Sidorkewicj et al., 1998) thus making these habitats suitable to use red or orange fluorescent lures.

According to Sidorkewicj et al. (1998), tubidity induced by carps may achieve 100-140 NTU.

Note also, turbidity induced by carps decreases angler catch rates of other sport fish (Drenner et al., 1997).

Basic references

Breden F., Stoner G. 1987. Male predation risk determines female preference in the Trinidad guppy. Nature 329, 831-833

Catalano M.J., Chipps S.R., Bouchard M.A., Wahl D.Y. 2001. Evaluation of injectable fluorescent tags for marking centrarchid fishes: Retention rate and effects on vulnerability to predation. North American Journal of Fisheries Management 21, 211-217

Cortemeglia C., Beitinger T.L. 2006. Susceptibility of transgenic and wildtype zebra danios, Danio rerio, to predation. Environmental Biology of Fishes 76, 93-100

Darkov A.A. 1980. Ecological features of visual signalization in fishes. Science Publishing, Moscow

Drenner R.W., Gallo K.L., Edwards C.M., Rieger K.E., Dibble E.D. 1997. Common carp affect turbidity and angler catch rates of largemouth bass in ponds. North American Journal of Fisheries Menagement 17, 1010-1013

Dugas M.B., Franssen N.R. 2011. Nuptial coloration of red shiners (Cyprinella lutrensis) is more intense in turbid habitats. Naturwissenschaften DOI 10.1007/s00114-011-0765-4

Gong Z., Wan H., Tay T.L., Wang H., Chen M., Yan T. 2003. Development of transgenic fish for ornamental and bioreactor by strong expression of fluorescent proteins in the skeletal muscle. Biochemical and Biophysical Research Communications 308, 58–63

Greany P.D., Burditt A.K., Agee H.R., Chambers D.L. 1978. Increasing effectiveness of visual traps for the Caribbean fruit fly, Anastrepha suspensa (Diptera: Tephritidae), by use of fluorescent colors. Entomologia Experimentalis et Applicata 23, 20-25

Hawryshyn C.W., Arnold M.G., McFarland W.N., Loew E.R. 1988. Aspects of color vision in bluegill sunfish (Lepomis macrochirus): ecological and evolutionary relevance. Journal of Comparative Physiology A164, 107-116

Hill J.E., Kapuscinski A.R., Pavlowich T. 2011. Fluorescent transgenic zebra danio more vulnerable to predators than wild-type fish. Transactions of the American Fisheries Society 140, 1001-1005

Hope J. 1984. The well-lured trout. Science 84, 160-167

Jha P. 2010. Comparative study of aggressive behaviour in transgenic and wildtype zebrafish Danio rerio (Hamilton) and the flying barb Esomus danricus (Hamilton), and their susceptibility to predation by the snakehead Channa striatus (Bloch). Italian Journal of Zoology 77, 102-109

Kawamura G., Kishimoto T. 2002. Color vision, accomodation and visual acuity in the largemouth bass. Fisheries Science 68, 1041-1046

Kelley J.L., Phillips B., Cummins G.H., Shand J. 2012. Changes in the visual environment affect colour signal brightness and shoaling behaviour in a freshwater fish. Animal Behaviour 83, 783-791

Kinney J.A.S., Luria S.M., Weitzman D.O. 1967. The visibility of colors underwater. Journal of the Optical Society of America 57, 802-807

Lescheva T.S., Zhuykov A.Y. 1989. Learning in fish. Ecological and applied aspects. Moscow, Science

Miller R.J., Janzow F.T. 1979. An experiment on visual discrimination in the largemouth bass, Micropterus salmoides. Proceedings of the Oklahoma Academy of Science 59, 34-40

Pocklington R., Dill L.M. 1995. Predation on females or males: who pays for bright male traits? Animal Behaviour 49, 1122-1124

Protasov V.R. 1978. Fish behaviour. The mechanisms of fish orientation and their use in fishing. Food Industry Publishing, Moscow

Richardson M.J., Whoriskey F.G., Roy L.H. 1995. Turbidity generation and biological impacts of an exotic fish Carassius auratus, introduced into shallow seasonally anoxic ponds. Journal of Fish Biology 47, 576-585

Roberts J., Chick A., Oswald L., Thompson P. 1995. Effect of carp, Cyprinus carpio L., an exotic benthivorous fish, on aquatic plants and water quality in experimental ponds. Marine and Freshwater Research 46, 1171-1180

Roberts J.H., Kilpatrick J.M. 2004. Predator feeding preferences for a benthic stream fish: effects of visible injected marks. Journal of Freshwater Ecology 19, 531-538

Seehausen O., van Alphen J.J.M., Witte F. 1997. Cichlid fish diversity threatened by eutrophication that curbs sexual selection. Science 277, 1808-1811

Sidorkewicj N.S., López Cazorla A.C., Murphy K.J., Sabbatini M.R., Fernandez O.A., Domaniewski J.C.J. 1998. Interaction of common carp with aquatic weeds in Argentine drainage channels. Journal of Aquatic Plant Management 36, 5-10

Utne-Palm A.C. 2002. Visual feeding of fish in a turbid environment: physical and behavioural aspects. Marine and Freshwater Behaviour and Physiology 35, 111–128

Animal responses to holographic patterns

In ethological literature, little is known about responses of fish and other animals to holographic foils which may be used in decoration of nests, sexual and schoolmate dummies, artificial fishing lures and other objects. To our knowledge, Östlund-Nilsson & Holmlund (2003) offered colored metal foil sticks (15 mm length) to males of three-spined stickleback, Gasterosteus aculeatus, to decorate their nests and found that males preferred sticks of red color. Even earlier, Darkov (1980) studied schooling behaviour of sunbleak, Leucaspius delineatus, and found that fish preferred to school with the silvery models than with the black models. However, in both these works the influence of holographic patterns on the behavioural responses of fish has not been studied. Experimental procedure Our experiments were carried out in an aquarium of 30 x 30 x 60 cm sizes under the daylight illumination. The aquarium bottom was covered with the pebbles of medium size (10-15 mm). At the distance of 3 cm from the side wall the lifting transparent glass was located. This glass was used to stick holographic models (see below). At the distance of 10 cm from this glass the frosted lifting glass was located. When animals moved near this glass, this glass was lifted and animals could see models. This tank was used as aquarium to study fish and as terrarium to study lizards. The experimental fish were wild perch, Perca fluviatilis (5-7 cm total length), wild roach, Rutilus rutilus (5-7 cm total length), and wild sunbleak, L. delineatus (about 4 cm total length). Fish were fed live bloodworms. The experimental lizards were sand lizards, Lacerta agilis (6-8 cm total length), which were fed live room flies and small grasshoppers (without one wing or one hind leg). When animals discovered models, they usually moved towards these models. Three types of responses were fixated: 1) the first movement to the left or right model, 2) staying near the left or right model during 30 min, and 3) the first attempt to bite the left or right model. As animals observed both models at the same time for free choice, the method of paired comparisons (sign test) was used for statistics. To make models, holographic foils produced by WTP Inc., USA (http://www.wtp-inc.com/color-card) were used. Small holograpic fields Fish The sizes of models were 20 x 5 mm. Two models were placed horizontally at the distance of 10 cm from each other, at the height of 5 cm from the bottom and at the distance about 12-14 cm from the fish. In the experiments of this type with perch and roach, the left model made of red plain foil, WTP 45, and the right model made of red holographic foil with large horizontal streaks, WTP 825, were compared. In all experiments with permutation models from left to right and vice versa, perch and roach preferred to approach, stay and bite without hesitations the holographic model over the plain model (sign test, P < 0,01). However, fish were no able to discriminate models with the similar holographic patterns like red prism glitter, WTP 355, and red mini scale, WTP 185. In general, fish can be trained to discriminate visual abstract patterns (for review, see Northmore et al., 1978), illusory patterns (Wyzisk & Neumeyer; 2007; Sovrano & Bisazza, 2009; Agrillo et al., 2013), mirror patterns (Gierszewski et al., 2013) and naturalistic forms (Schluessel et al., 2012). However, in our experiments wild perch and roach were untrained for the aims of visual discriminations and generalized similar holograpic patterns. Lizards Because lizards are more sensitive to the light of shorter wavelengths, models of blue color were used. Models made of blue plain foil, WTP 43, and blue holographic foil with large horizontal streaks, WTP 823, were compared. In all cases, lizards preferred the holographic model over the plain model (sign test, P < 0,01). However, lizards were no able to discriminate models with the similar holographic patterns like blue prism glitter, WTP 353, and blue mini scale, WTP 183. Basic wooden decoys In this part of the experiments, we considered how predatory fish responded in the field to the plain foils and holographic foils with the different patterns. Basic wooden decoys are lathed practically of any timber, including an imported balsa, and have not any concavities. Commonly, lures have an usable cylindric shape (with the flat or roundish ends), an elongated oval shape, an elongated barrel-like shape (with the flat ends) and an elongated drop-like shape (with the most diameter in the tail, near to the hook). Decoys do not equipped with self-righting ventral hooks, so their rostrums have not skews for sinking or lifting. To use 2D & 3D artificial eyes, recesses with the flat bottom are milled in the decoy bodies. Each decoy has the central longitudinal hole and is strung directly on the fishing line, resting on the treble hook. To fish pike, Esox lucius, with sharp teeth, steel leaders are used. The treble hook is decorated with the woolen or synthetic material, commonly of white or light grey colors. In our experiments, waterproof cylindric wooden decoys of 5.0 cm length and 1.0 cm diameter were used. Their bodies were enveloped with silvery plain foils and sivery holographic foils described below. In addition, 2D eyes 7/32” with the red iris, WTP 405, were sticked bilaterally in the head part of all decoys. Compared decoys were tested in pairs using standard trolling technique on the two sides of the boat at the same time. Trolling was carried out in daytime at the depth 2.5-3.0 m. The distance between moving decoys was about 2 m. Visibility in the water was 0.6-0.8 m for Secchi disk. Thus fish could not see both compared lures simultaneously and therefore independent samples were used for statistics. The most abundant predatory fish like perch, P. fluviatilis, pikes, E. lucius, zanders, Stizostedion lucioperca, and asps, Aspius aspius, were catched and considered in the general pool. In an aquarium when two flat foil stripes (20 x 5 mm) are static, perch have enough time to study both models and prefer (sign test, P < 0,01) the silvery holographic foil with prism glitter, WTP 351, over the silvery plain foil, WTP 41. In the field, however, perch and other predatory fish are forced to attack potential prey very quickly (during split second) and thus they have not enough time to study their visual features. So approximately the same number of perch, pike, zander and asp (Table 1) were caught on decoys enveloped with the plain and holographic foils or with the different holographic foils. In general (see Curio, 1976), the process of prey-recognition (seconds, minutes, hours) and the process of prey-attack (split second) are the different processes that are separated in time. Species Caught fish number Stimulus #1 (silvery) Stimulus #2 (silvery) Statistics (n fish per 1 hour of trolling, Student’s t-test) perch, pike, zander, asp 32 prism glitter, WTP 351 without glitter, WTP 41 indifferently perch, pike, zander, asp 21 horizontal lines, WTP 341 vertical lines, WTP 341 indifferently perch, pike, zander, asp 27 stripes tilted to the left, WTP 201 stripes tilted to the right, WTP 201 indifferently Table 1. The results of predatory fish catching in the field on decoys decorated with the plain and holographic foils. Dodgers and flashers Oscillating dodgers and rotating flashers are special trolling devices. They have large sizes (up to 30 cm) and are frequently equiped with the holographic foils (Fig 1). Fig. 1. Trolling flashers with the holographic foils. Trolling gears with dodgers allow to catch predatory fish of larger sizes than gears without dodgers (Dooley, 1989). It means that strongly vibrating and shining dodgers and flahers repel relatively small predatory fish. Nothing is known about the effect of holographic patterns. Medium holographic fields In the experiments of this type, rectangular models, 4 x 1 cm, and sunbleak (about 4 cm length) had approximately equal sizes to study schooling responses of fish. Three randomly placed horizontal models made of silvery plain foil, WTP 41, and three randomly placed horizontal models made of silvery holographic foils with prism glitter, WTP 351, were compared. In all cases, highly schooling sunbleak (1, 2 and 3 individuals) preferred to approach and to stay near the holographic models over the plain models (sign test, P < 0,01). However, sunbleak were no able to discriminate models with the similar holographic patterns like silvery prism glitter, WTP 351, and silvery mini scale, WTP 181. Large holographic fields In these cases, the sizes of holographic objects are much more than the sizes of the experimental animals. The rectangular photos (20 x 10 cm) of underwater plants and rectangular photos of grass at the level of sand on the one hand, and the holographic panels (20 x 10 cm) of the various types on the second hand were used to study the responses of fish and lizards, respectively. Fish and lizards were introduced individually in aquarium or terrarium in the center between photos and holographic panels and released. In all cases, fish and lizards moved immediately or after short confusion towards the natural backgrounds avoiding thus the large holographic panels (sign test, P < 0,01). All holographic patterns scare. In other words, fish and lizards are not able to distinguish scared holographic patterns. These results are not new. It is known, for example, that holographic foils are repellents for birds and produced on an industrial scale (see https://www.shopwtp-inc.com/index.php?cPath=34). Basic references Agrillo C., Petrazzini M.E.M., Dadda M. 2013. Illusory patterns are fishy for fish, too. Frontiers in Neural Circuits 7, doi: 10.3389/fncir.2013.00137 Curio E. 1976. Ethology of predation. Zoophysiology and Ecology 7. Berlin, Springer Darkov A.A. 1980. Ecological features of visual signalling in fishes. Moscow, Science Publishing Dooley R.H.A. 1989. The response of rainbow trout (Salmo gairdneri) to lures with special reference to color preference. Master’s Thesis. University of British Columbia, Canada, 1-76 Gierszewski S., Bleckmann H., Schluessel V. 2013. Cognitive abilities in malawi cichlids (Pseudotropheus sp.): matching-to-sample and image/mirror-image discriminations. PLoS ONE 8: e57363. doi:10.1371/journal.pone.0057363 Northmore D., Volkmann F.C., Yager D. 1978. Vision in fishes: color and pattern. The Behavior of Fish and Other Aquatic Animals. Edited by D.I. Mostofsky. Academic Press, New York Östlund-Nilsson S., Holmlund M. 2003. The artistic three-spined stickleback (Gasterosteus aculeatus). Behavioral Ecology and Sociobiology 53, 214-220 Schluessel V., Fricke G., Bleckmann H. 2012. Visual discrimination and object categorization in the cichlid Pseudotropheus sp. Animal Cognition 15:525-537 Siebeck U.E., Litherland L., Wallis G.M. 2009. Shape learning and discrimination in reef fish. Journal of Experimental Biology 212, 2113-2119 Sovrano V.A., Bisazza A. 2009. Perception of subjective contours in fish. Perception 38, 579-590 Wyzisk K., Neumeyer C. 2007. Perception of illusory surfaces and contours in goldfish. Visual neuroscience 24, 291-298