Visual amimetic stimuli: An antroduction

General Studying behavioural responses of animals in experimental conditions, ethologists have found relatively simple stimuli that could be more effective than the natural objects. Single spots (called also eye-spots) and two horizontally arranged spots, rectangular longitudinal stripes, periodic gratings and other stimuli (Fig.1) belong to them. Because the foregoing stimuli are not exact imitations of the natural objects, we will call them amimetic stimuli. In several articles, we will group the main visual amimetic stimuli and describe how they are used in the ethological research, whether they occur in the nature as well as their application in the fishing lure industry. In the framework of applied ethology, we will address to the fishing lure industry. It is that only sphere of the human activites, where artificial stimuli and models of the various animals are used in the largest scale. Figure 1. The basic visual amimetic stimuli Names of the basic visual amimetic stimuli used in this article: 01. Concentric spots 02. Two horizontal spots 03. 2D & 3D roundish stimuli 04. Rectangular stripes 05. Periodic gratings 06. Chains 07. Vibrators 08. Spinners (rotating stimuli) 09. Flutters 10. Undulators 11. Pulsators 12. Mechanical & light flashers Note, stimuli 05 and 06 are periodic spatial, whereas stimuli 07, 08, 09, 10, 11, and 12 are periodic spatiotemporal In the terminology of early ethologists, some of the amimetic stimuli shown above called the sign stimuli (e.g., Manning & Dawkins, 1998). Generally, using simple stimuli and changing parts of complex stimuli, scientists were able to find the so called supernormal stimuli that induced in animals the more strong behavioural responses than the modelling natural objects. For example, the giant cane toads, Bufo marinus, respond to the horizontally moving rectangular longitudinal stripes (20 mm long x 2.5 mm high) much more actively (on average of 10 times) than to live crickets and insect plastic models (Robins & Rogers, 2004). Similarly, reproductive males of the common toad, Bufo bufo, prefer (in four cases against one) to form sexual pairs (Fig.2) with the fixed blue discs (5 cm diameter) than with the live mobile females (Gnyubkin & Kondrashev, 1978). Figure 2. Reproductive males of toads prefer to congregate sexual pairs with blue discs than with live females Manning and Dawkins (1998) give many other examples of this kind. Neuroethology Visual amimetic stimuli induce numerous behavioural responses in many animals and do not imitate, as mentioned above, the concrete natural objects. The effectiveness of these stimuli is grounded on the common mechanisms of visual perception, common for all visually guided animals. Among visual amimetic stimuli, the nature of spots, stripes and gratings, both static and moving, as well as rotating striped drums is most studied. For example, in fish and other vertebrate animals, spots are detected at the level of ganglion cells of retina, which have the more or less distinct concentric receptive fields with the antagonistic center and periphery. According to Horn (1962; see Fig. 6.5 b,c), the boundaries of some spot are distinguished depending on its size by one or several ganglion cells with the foregoing receptive fields. Rectangular stripes and periodic gratings appeared in the field of view are detected by the so called orientation selective ganglion cells (e.g., Damjanović et. al., 2009). It is shown in numerous electrophysiological tests that the cells of this type are represented by two relatively distinct units called, respectively, the detectors of horizontal lines and the detectors of vertical lines. In addition, on an example of developing larval zebrafish, Brachydanio (Danio) rerio, as an usable model object, neuromotor grounds of the behavioural responses to artificial and natural visual stimuli are studied, in the larva development (for review, see Portugues & Engert, 2009): 1) responses to large-filed moving vertical gratings, called optomotor responses 2) responses to live parameciums and small moving spots, called prey tracking 3) responses to large moving spots and other large objects, called escape responses Among other mechanisms of adjusted effectiveness of amimetic visual stimuli matched with the corresponding receptive fields, bilateral symmetry of spots and spatial symmetry of gratings play an exceptionally inportant role (e.g., Kenward et al., 2004). The effectiveness of pair stimuli is determined by the bilateral symmetry of visual system and visual perception evolving during millions of years in the field of the Earth gravitation, but the causes of the evolution of repetitive stilmuli and the corresponding receptive fields are unclear. Kenward et al. (2004) consider about ten factors that might lead to the evolution of repetitive visual stimuli and the corresponding receptive fields, including the highest detectableness of repetitive stimuli on the background of environmental optic noises. In addition to spatial amimetic visual stimuli, there are more complex spatiotemporal amimetic visual stimuli (for review, see, e.g., Rothental, 2007). In fish, responses to such spatiotemporal stimuli as rhythmic (temporal symmetric) pulsations, vibrations and (worm-like) undulations are innate. In contrast to the spatial periodic gratings (Damjanović et al., 2009), there are not distinct receptive units to detect these complex stimuli. Basic References Damjanović I., Maximova E.M., Maximov V.V. 2009. On the organization of receptive fields of orientation-selective units recorded in the fish tectum. Journal of Integrative Neuroscience 8, 323–344 Gnyubkin V.F., Kondrashev C.L. 1978. Pair aggregation in the common toad, Bufo bufo L., in the reproductive period. In: Mechanisms of animal vision. Moscow, Science, 40-75 Horn G. 1962. Some neural correlates of perception. Viewpoints in Biology. Butterworth & Co. Publishers, London, p. 240-285 Kenward B., Wachtmeister C. A., Ghirlanda S., Enquist M. 2004. Spots and stripes: the evolution of repetition in visual signal form. Journal of Theoretical Biology 230, 407-419 Manning A., Dawkins M.S. 1998. An introduction to animal behaviour. 5th editon. UK, Camdridge University Press Portugues R., Engert F. 2009. The neural basis of visual behaviors in the larval zebrafish. Current Opinion in Neurobiology 19, 1–4 Robins A., Rogers L.J. 2004. Lateralized prey-catching responses in the cane toad, Bufo marinus: analysis of complex visual stimuli. Animal Behaviour 68, 567-575 Rothental G.G. 2007. Spatiotemporal dimensions of visual signals in animal communication. Annual Review of Ecology, Evolution and Systematics 38, 155–78

Ultraviolet colors in fishing lures

Rapala VMC Corporation manufactures and sells artificial fishing lures with the ultraviolet (UV) finishes that combine fluorescent paints, reflective surfaces and optical brighteners (see http://rapala.fishing/lure-finishes). Lures with theses finishes are marked by signs “UV BRIGHT” or simply “UV”. However, Rapala does not understand the abilities of ultraviolet (with the wavelength below 400 nm) vision in fish and its role in their responses to UV reflected objects in the nature and fishing.

Fig. 1. The sigh used by Rapala (brands Rapala, Storm, Blue Fox and Luhr Jenssen) to mark the lures with the UV finishes.

UV finishes in mafacturing fishing lures are also used by other companies like Lakeland Inc., USA (see http://lakelandinc.com/UFI/UFI_vibrant.html).

Ultraviolet vision

Freshwater fish

Numerous freshwater small-sized fish like three-spined stickleback, Gasterosteus aculeatus, reflect (Rick et al., 2004) radiation in the ultraviolet part of the electromagnetic spectrum and have UV vision. In particular, three-spined stickleback use UV vision in schooling (Modarressie et al., 2006), sexual (Rick & Bakker, 2008) and foraging (Rick et al., 2012) behavioural responses. The similar results are found for guppy, Poecilia reticulata (Smith et al., 2002), sailfin molly, P. latipinna (Palmer & Hankison, 2015), and other freshwater small-sized fish in the adult age.

However, UV reflection by some body does not provide the success per se. For example, during the nest decoration in artificial conditions males of three-spined stickleback choose rather red foil strips which absorb UV radiation than silvery or blue foil strips which reflect UV radiation (Östlund-Nilsson & Holmlund, 2003).

In turn, yearlings of predatory brown trout, Salmo trutta, use UV reflection of three-spined stickleback to hunt these prey (Modarressie et al., 2013). However, only young trout are sensitive to UV (see data by Bowmaker & Kunz, 1987, for Salmo trutta; Hawryshyn et al., 1989, for Salmo gairdneri), while older (over two years) fish lose this ability.

The same ontogeny of UV vision is typical for other freshwater predatory fish like perch and others (see Bowmaker, 1990). With the age, the ocular structures change radically and do not allow the fish to perceive UV radiation.

Saltwater fish

Great care must be taken in relation to marine fish and invertebrates (like crustaceans) many of which have UV vision (Losey & Cronin, 1997; Siebeck & Marshall, 2001; Losey et al., 2003).

According to Fritsches et al. (2000), marine predatory fish of the younger age groups and medium-sized fish (like slimy mackerel, Scomber australasicus, and others) are sensitive to UV, while marine predatory fish of the older age groups and large-sized fish (like blue marlin, Makaira nigricans, black marlin, Makaira indica, sailfish, Istiophorus platypterus, and others) are UV blind.

In general, UV signals are mainly used by small-sized and juvenile fish (both freshwater and saltwater) to form private communuication channels that are relatively inaccessible for potential predators (Siebeck, 2014).

Thus, UV finishes of Rapala’s lures and lures of other companies are useless for freshwater and saltwater predatory fish of the older age groups which lose UV vision with the age.

Optical brighteners

In addition to reflective surfaces, Rapala uses optical brighteners. The use of optical brighteners  complicates the description of the optical properties of UV fishishes.

It is well known that optical brighteners are fluorescent substances which absorb UV radiation and immediately re-emit it in the visible part of the spectrum with the maximun of re-emission in violet and blue parts of the spectrum. White covers with optical brightners reflect partly the falling sun light which is mixed with the light of fluorescence, so the human’s eye perceives these covers as “more bright” and “more white” (well known as “snow white”) than white covers without optical brighteners.

In the pure form, fluorescent white finishes are used, for example, by Lakeland Inc. to cover its metal spoons and spinners (see http://www.lakelandinc.com/finishes.html).

In general, white and fluorescent white colors are most visible in the freshwater and saltwater environments (Kenney et al., 1967, 1968). But the great visibility of white and fluorescent white colors does not guarantee their attractiveness for fish.

For example, Dooley (1989) has studied using trolling technique the responses of rainbow trout, Salmo gairdneri, to wobblers, spoons and spinners of various colors and found that lures of the solid white color were less effective than lures of blue, green, yellow and red colors. Moraga et al. (2015) have studied using sink-and-retrieving technique the responses of largemouth bass, Micropterus salmoides, to soft plastic worms (of 12.7 cm length) of various colors and found that worms of the “pearl white” color were less effective than worms of natural and dark colors.

The same results were obtained in marine fishing. For example, according to Hsieh et al. (2001), in mackerel longline fishing white lures were slightly more effective than blue, purple and transparent lures (cryptic on the background of marine column) but less effective than black and red lures.

Psychological perception of white objects

It is known that relatively large objects of white color may scare fish. So, Moraga et al. (2015) have found that white soft plastic worms of 12.7 cm length allow to catch largemouth bass of greater sizes than the same worms of darker colors. It means that white lures warn of danger or scare largemouth bass of smaller sizes.

In general, white objects are perceived greater in size than the same dark objects (e.g., Kremkow et al., 2014).

On the other hand, because the natural sun light contains all the chromatic colors, which may be detected with the assistance of Newton’s lens, we perceive the sun light as “white”. In the same manner, we perceive any white surfaces (like white clouds, snow, paper, etc.) as “white” because these surfaces reflect more or less evently all components of the sun light.

However, our perceptions can not be automatically transferred to fish perceptions!

It is known that fresh water absorbs short-wavelength rays and transmits long-wavelength rays, so the maximum of spectral sensitivity of eyes of freshwater fish is shifted to the orange and red parts of the optical spectrum (e.g., Tamura & Niwa, 1967). Therefore, the “white light” for freshwater fish is enriched with the long-wavelength rays (we name this light as “worm light” or “warm white”). In contrast, marine water absorbs long-wavelength rays and transmits short-wavelength rays, so the maximum of spectral sensitivity of eyes of saltwater fish is shifted to the blue and green parts of the optical spectrum (Tamura & Niwa, 1967). Therefore, the “white light” for saltwater fish is enriched with the short-wavelength rays (we name this light as “cool light” or “cool white”).

How fish perceive colors, see Vorobyev et al. (2001).

In addition, for small-sized and juvenile freshwater and salwater fish the “white light” is enriched with UV rays (see above), which are invisible for the human’s eye.

Numerous freshwater and saltwater fish have white or whitish with the different tints belly (or the lower side in flat fish) that masks them on the backgrounds of the bright water surface illuminated with the sun light. Subjected to the conditions of crypsis in the water environment, boldly white fish (like arctic animals in winter) are absent in this environment, excepting white morphs.

In order to estimate roughly the composition of the underwater light, you must check first of all the ventral coloration in fish, that is the coloration of their bellies. For example, in such fish as carp, Cyprinis carpio, tench, Tinca tinca, and other ecologically close fish, which live in the strongly eutrophicated and colored fresh waters, the ventral coloration is characterized by yellowish, olivish, orangish, brownish or even reddish tints (e.g., see colored images of freshwater peacock bass, Cichla temensis: Reiss et al., 2012). Namely these colors and tints define at the first approach the composition of the underwater light under the foregoing optical conditions.

Because for freshwater fish red color is most lighter than all others, red colors and tints occur widely in coloration of their lower fins (this phenomenon is called colored countershading).

Whitish ventral coloration is observed only in pelagic and, partly, in demersal freshwater fish. Snow white ventral coloration occurs only in pelagic saltwater fish.

In conclusion, Rapala and Lakeland companies do not give the reflectance spectra of their finishes. There not any statistic data confirmed the effectiveness of lures with these finishes to catch more fish.

Basic references

Bowmaker J.K. 1990. Visual pigments of fishes. In: The visual system of fishes. Edited by Douglas R.H. & Djamgoz M.B.A. Chapman & Hall, London, 81–107

Bowmaker J.K., Kunz Y.W. 1987. Ultraviolet receptors, tetrachromatic colour vision and retinal mosaics in the brown trout (Salmo trutta): Age-dependent changes. Vision research 27, 2101-2108

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

Fritsches K.A, Partridge J.C., Pettigrew J.D., Marshall N.J. 2000. Colour vision in billfish. Philosophical Transactions of the Royal Society B: Biological Sciences 29, 1253-1256

Hawryshyn C.W., Arnold M.G., Chaisson D.J., Martin P.C. 1989. The ontogeny of ultraviolet photosensitivity in rainbow trout (Salmo gairdneri). Visual Neuroscience 2, 247-254

Hsieh K.Y., Huang B.Q., Wu R.L., Chen C.T. 2001. Color effects of lures on the hooking rates of mackerel longline fishing. Fisheries Science 67, 408-414

Kinney J.A.S., Luria S.M., Weitzman D.O. 1967. Visibility of colors underwater. U.S. Naval Submarine Medical Center. Report Number 503

Kinney J.A.S., Luria S.M., Weitzman D.O. 1968. The underwater visibility of colors with artificial illumination. U.S. Naval Submarine Medical Center. Report Number 551

Kremkow J., Jin J., Komban S.J., Wang Y., Lashgari R., Li X., Jansen M., Zaidi Q., Alonso J.M. 2014. Neuronal nonlinearity explains greater visual spatial resolution for darks than lights. Proceedings of the National Academy of Sciences 111, 3170-3175

Losey G.S., Cronin T.W. 1997. The UV visual world of fishes. Proceedings of the 5th Indo-Pacific Fish Conference: Noumea, New Caledonia, 819-826

Losey G.S., McFarland W.N., Loew E.R., Zanzow J.P., Nelson P.A., Marshall N.J. 2003. Visual biology of Hawaiian coral reef fishes. I. Ocular transmission and visual pigments. Copeia 2003, 433-454

Modarressie R., Rick I.P., Bakker T.C.M. 2006. UV matters in shoaling decisions. Proceedings of the Royal Society B273, 849-854

Modarressie R., Rick I.P., Bakker T.C.M. 2013. Ultraviolet reflection enhances the risk of predation in a vertebrate. Current Zoology 59, 151-159

Moraga A.D., Wilson A.D.M., Cooke S.J. 2015. Does lure colour influence catch per unit effort, fish capture size and hooking injury in angled largemouth bass? Fisheries Research 172, 1–6

Östlund-Nilsson S., Holmlund M. 2003. The artistic three-spined stickleback (Gasterosteus aculeatus). Behavioral Ecology and Sociobiology 53, 214-220

Palmer M.S., Hankison S.J. 2015. Use of ultraviolet cues in female mate preference in the sailfin molly, Poecilia latipinna. Acta Ethologica 18, 153–160

Reiss P., Kenneth W. Able K.W., Nunes M.S., Hrbek T. 2012. Color pattern variation in Cichla temensis (Perciformes: Cichlidae): Resolution based on morphological, molecular, and reproductive data. Neotropical Ichthyology 10, 59-70

Rick I. P., Bakker T.C.M. 2008. UV wavelengths make female three-spined sticklebacks (Gasterosteus aculeatus) more attractive for males. Behavioral Ecology and Sociobiology 62, 439-445

Rick I.P., Bloemker D., Bakker T.C.M. 2012. Spectral composition and visual foraging in the threespine stickleback (Gasterosteidae: Gasterosteus aculeatus L.): Elucidating the role of ultraviolet wavelengths. Biological Journal of the Linnean Society105, 359-368

Rick I.P., Modarressie R., Bakker T.C.M. 2004. Male three-spined sticklebacks reflect in ultraviolet light. Behaviour 141, 1531-1541

Siebeck U.E., Marshall N.J. 2001. Ocular media transmission of coral reef fish  can coral reef fish see ultraviolet light? Vision research 41, 133-149

Siebeck U.E. 2014. Communication in the ultraviolet: Unravelling the secret language of fish. In: Biocommunication of animals. Edited by Guenther Witzany, Springer, 299-320

Smith E.J., Partridge J.C., Parsons K.N., White E.M., Cuthill I.C., Bennett A.T.D., Church S.C. 2002. Ultraviolet vision and mate choice in the guppy (Poecilia reticulata). Behavioral Ecology 13, 11-19

Tamura T., Niwa H. 1967. Spectral sensitivity and color vision of fish as indicated by S-potential. Comparative Biochemistry and Physiology 22, 745-754

Vorobyev M., Marshall J., Osorio D., de Ibarra N.H., Menzel R. 2001. Colourful objects through animal eyes. Color Research & Application 26, S214-S217