Surface wave detection by animals: Difference between revisions

[[File:Aplocheilus lineatus Day.png|thumb|300px|right|Most research on the detection of surface waves has been done on the [[striped panchax]], ''Aplocheilus lineatus'']]

'''Surface wave detection by animals''' is the process by which animals, such as surface-feeding fish are able to sense and localize [[prey]] and other objects on the surface of a body of water by analyzing features of the ripples generated by objects' movement at the surface. Features analyzed include [[waveform]] properties such as [[frequency]], change in frequency, and [[amplitude]], and the curvature of the [[wavefront]]. A number of different species are proficient in surface wave detection, including some aquatic insects and toads, though most research is done on the topminnow/surface killifish ''[[Aplocheilus lineatus]].'' The fish and other animals with this ability spend large amounts of time near the water surface, some just to feed and others their entire lives.

==Description of behavior==

Certain species of fish spend a substantial portion of their lives near the surface of the water in order to feed, usually on insects that are struggling at the surface. Species that detect surface waves typically use them to localize such prey. When the hunting posture is assumed (which may be neutral posture) as specific mechanosensitive organ is held in contact with the surface of the water in order that mechanoreceptors can receive surface waves. The animal will wait a small amount of time (typically <1s) before initiating a response towards the prey, should the surface waves perceived fall within the preferred stimulus range. Response towards prey typically follows the pattern orientation towards prey, swimming towards prey, and then prey capture. This ability is sometimes referred to as a sense of "distant touch."<ref name="Schwarz et al., 2011">Schwarz, J.S., Reichenbach, T., and Hudspeth, A. J. (2011) "A hydrodynamic sensory antenna used by killifish for nocturnal hunting". ''The Journal of Experimental Biology'' 214:1857-1866</ref>

Several species have been shown to use surface wave detection for prey capture. Among these are many species of freshwater fish, notably the groups hatchetfish ([[Freshwater hatchetfish|Gasteropelecidae]]), freshwater butterflyfish ([[Pantodontidae]]), halfbeaks ([[Hemiramphidae]]) and killifish ([[Aplocheilidae]])(list from <ref name="Schwarz et al., 2011" />). For its consistently stellar performance at the task, the topminnow/killfish (both terms are used in the literature) is one of the primary models for investigation. These species tend to live in small bodies of freshwater, as well as creeks and swamps.

==Surface waves==

[[File:Ripples Lifjord.jpg|thumb|right|Capillary wave ripples on Lifjord in [[Øksnes]], Norway]]

{{see also|Capillary wave}}

The ripples which surface-feeding fish detect are known more technically as capillary waves. Capillary waves are generated by movement of an object at the surface of the water or from the brief contact of an object with the surface from either medium (air or water). Waves radiate outward in concentric circles from the source, and the waveform of each train of waves changes in very specific and predictable waves, as dictated by surface tension and gravity.<ref name="Bleckmann and Kase, 1987">Bleckmann H, and Kase R. H. (1987) "Prey localization by surface wave ray-tracing: fish track bugs like oceanographers track storms". ''Experientia'' 43: 290-293</ref> The water surface has a dampening effect which causes an abnormal dispersion pattern in which waves decrease in amplitude, speed and frequency with distance from the source.<ref name="Bleckmann and Kase, 1987" /><ref name="Müller and Schwartz, 1982">MüllerU., and Schwartz E. "Influence of single neuromasts on prey localizing behavior of surface-feeding fish, Aplocheilus lineatus". ''Journal of Comparative Physiology'' A 149 (1982): 399-408</ref> Short-wavelength (higher frequency) waves disperse faster than longer wavelength waves, resulting in higher frequencies at the front of the wave-train and lower frequencies at the tail; a fish detects this as a downward-sweeping frequency modulation.<ref name="Bleckmann and Kase, 1987" />

{{clear}}

A vast amount of the research on surface wave detection has been done in the surface-feeding topminnow/killfish ''[[Aplocheilus lineatus]]''. Schwartz (1965) demonstrated that this species has exceptionally well-developed surface wave detection ability, and it is easily housed and trained in laboratories.<ref name="Schwartz, 1965">Schwartz, E. (1965) "Bau und Funktion der seitenlinie des streifenhechtlings Aplocheilus lineatus". "Z Vergl Physiology A 50": 55-87, cited and translated in Coombs S., Görner P., and Münz H. eds. ''The Mechanosensory Lateral Line: Neurobiology and Evolution'' (New York: Springer-Verlag New York Inc., 1989), pp.501-524</ref> [[Pantadon bucholzi]] (a surface dwelling butterfly fish) is used less often though is very similar in its anatomy and behavior. The rest of this article will focus on research done with ''A lineatus''.

''(See the work of Bleckmann, Schwartz, Müller, etc., 1965-present).''

Wave characteristics are measured optically. This is done by shining a laser (often helium-neon) at the water surface. Reflections and distortions of the laser's beam are picked up by a photodiode.

Fishes' movements are videotaped with a high-speed camera from above the testing tank so that the precise timing and nature of their responses' to stimuli can be reviewed.

===Behavior of A lineatus===

''[[Aplocheilus lineatus]]'' assumes a hunting posture at the water surface in which it holds the top of its head within 200 μm of the water surface.<ref name="Schwarz et al., 2011" /> On perception of appropriate wave stimuli, fish first turn towards the stimulus.<ref name="Schwartz, 1965" /> This initial turn is made within 150ms of the wavetrain's arrival to the fish.<ref name="Schwarz et al., 2011" /> Fish then swim to the wave's source. There are specific parameters for wave stimuli to be perceived which reflect the type of waves produced by prey. Fish are least sensitive to low frequencies, with a minimum threshold of 10&nbsp;Hz and have peak sensitivity at 75–150&nbsp;Hz; the highest frequency they can detect is 250&nbsp;Hz.<ref name="Müller, 1984">Müller, U. (1984) "Die morphologie und physiologie Anpassung des Seitenlinien-systems von Pantodon bucholzo an den Lebensraum Wasseroberflache". PhD Thesis, University of Giessen, West Germany, cited in Coombs S., Görner P., and Münz H. eds. ''The Mechanosensory Lateral Line: Neurobiology and Evolution'' (New York: Springer-Verlag New York Inc., 1989), pp.501-524</ref> These waves have small amplitudes (on a micrometer-scale), and fish can detect waves with minimum peak-to-peak displacement of 1 μm at 10&nbsp;Hz and 0.0007μm in their most sensitive range of 75–100&nbsp;Hz. Fish are also sensitive to waves generated within 7–30&nbsp;cm of the fish's location, though they can occur at any point within that radius. Because the water surface acts as a low pass filter, this radius is different for different wave frequencies: 70&nbsp;Hz waves with 100μm peak-to-peak distance are subthreshold at 37&nbsp;cm, and 140&nbsp;Hz waves are subthreshold at 19&nbsp;cm.<ref name="Bleckmann, 1980">Bleckmann, H. (1980) "Reaction time and stimulus frequency in prey localization in the surface-feeding fish Aplocheilus lineatus". ''Journal of Comparative Physiology'' 140:163-172, cited in Hoin-Radkovsky, Bleckmann, Schwartz 1984)</ref> Fish are able to tell apart concurrent waves of different frequencies when the frequencies are different by at least 15%, though at certain frequencies this difference can be as low as 8%.<ref name="Hoin-Radkovsky et al., 1984">Hoin-Radkovsky, I., Bleckmann, H., and Schwartz, E. (1984) "Determination of the source distance in the surface-feeding fish Pantodon bucholzi pantodontidae". ''Animal Behavior'' 32:840-851</ref>

The wave-detection system of ''A lineatus'' and other surface feeding fish is tuned to match the waves that signal prey in their environment. ''A lineatus'' feeds on aquatic, semi-aquatic and terrestrial insects, often insects that have just touched the surface of the water or have fallen in and are struggling at the surface.<ref name="Hoin-Radkovsky et al., 1984" /><ref name="Bleckmann and Mohr, 1998" /> Abiotic sources give off capillary waves of frequency 8–14&nbsp;Hz, while biotic sources give off much higher frequencies, anywhere from 12–45&nbsp;Hz and above.<ref name="Bleckmann et al., 1981">Bleckmann, H., Waldner, I., and Schwartz, E. (1981) "Frequency Discrimination of the Surface-Feeding Fish Aplocheilus lineatus - A Prerequisite for Prey Localization?" ''Journal of Comparative Physiology'' 143:485-490</ref> This correlates well with ''A lineatus''' peak sensitivity at higher frequencies.

Wave stimuli are classified into two types: the first is click stimuli (short bursts of amplitude less than 100μm which contain many frequencies between 5&nbsp;Hz and 190&nbsp;Hz and are of short duration, as when an insect just touches the water rather than moves continuously at the surface).<ref name="Bleckmann, 1980" /> The other is continuous wave stimuli, which will contain many frequencies and in the wild are generated by fallen prey struggling at the water surface.<ref name="Hoin-Radkovsky et al., 1984" />

It has been pointed out that ''A lineatus'' and other surface feeding fish are able to locate prey even if the waveform is only in click form (just touching the surface once, as when surfacing for air or when a mosquito larva is hatching),<ref name="Lang, 1980" /> which takes less time to complete than the fish will take to swim over.<ref name="Bleckmann and Kase, 1987" /><ref name="Lang, 1980">Lang, H.H. (1980a) Surface wave discrimination between prey and nonprey by the back swimmer Notonecta glauca L. (Hemiptera, Heteroptera). Behavioral Ecology and Sociobiology 6:233-246, cited in Bleckmann, H, and Schwartz, E. (1982) "The functional significance of frequency modulation within a wave train for prey localization in the surface-feeding fish Aplocheilus lineatus". ''Journal of Comparative Physiology'' 145: 331-339</ref> This indicates that the fish are simply performing a form of sensory taxis, that they are getting all the information they need to locate the prey in the initial stimulus reception and are retaining the location while orienting and swimming. Fish also can begin orienting and swimming after receiving only the first few waves in a wavetrain or click stimulus.

When stimuli are presented within a detectable range, orientations toward the stimulus by ''A lineatus'' are extremely precise: the response is almost perfect with angles up to 150° in either direction from forwards, and precision falls off but not much when waves come from the rear of the fish.<ref name="Müller and Schwartz, 1982" />

There is some disagreement in the field about how ''A lineatus'' determines the direction of a stimulus. A common suggestion is that an animal performs a ray tracing calculation, similar to what human oceanographers use to locate ocean storms without a satellite.<ref name="Bleckmann and Kase, 1987" /> Theoretically, an animal could compare the arrival times of a wavetrain at two neuromasts, effectively measuring the curvature of the wavefront (the farther away the fish is from the source, the less arc angle will be measured in the distance between the neuromasts).<ref name="Bleckmann and Kase, 1987" /> However, there is no evidence of a neural circuit that performs this calculation, and other researchers suggest that the distance between any pair of surface wave neuromasts is too small (''A lineatus's'' head is only 1&nbsp;cm wide) for the calculation to be made accurately, and then at distances from the stimulus less than 7&nbsp;cm.<ref name="Bleckmann and Schwartz, 1982">Bleckmann, H, and Schwartz, E. (1982) "The functional significance of frequency modulation within a wave train for prey localization in the surface-feeding fish Aplocheilus lineatus". ''Journal of Comparative Physiology'' 145: 331-339</ref> The accuracy predicted by a time-difference mechanism (using triangulation of the wave source based on curvature of wave front) doesn't match actual accuracy.<ref name="Hoin-Radkovsky et al., 1984" /> Additionally it has been shown that if all neuromasts are removed except for one, direction detection still occurs to some degree,<ref name="Müller, 1981">Müller, U. (1981) "Der Einflulb einzelner Neuromasten des Seitenliniensystems auf die Lokalisationsleistung des Streifenhechtlings Aplocheilus Lineatus". Diplomarbeit, Universitat Giessen, FRG, cited in Bleckmann and Schwartz, 1982</ref>

An alternative theory is that individual neuromasts have a preferred direction, that is they are most sensitive to waves coming from a particular direction. A comparison of activation levels of different neuromasts is a relatively easy neural calculation to perform.

When neuromasts are removed unilaterally, fish still turn towards the side the stimulus came from though overestimate the angle by an average of 21° towards the side with intact neuromasts.<ref name="Müller and Schwartz, 1982" /> In this situation, fish often make two turns, first towards the side with intact neuromasts and then back towards the other.<ref name="Müller and Schwartz, 1982" />

Each neuromast has a preferred direction. This was shown in 1970 through ablation of all but one neuromast: fish then usually turned towards one range of directions regardless of where the stimulus came from.<ref name="Schwartz, 1970">Schwartz, E. (1970) Ferntastsinne yon Oberflachenfischen. Z Morphol Tiere 67:40-57, cited in Müller and Schwartz, 1982</ref> The direction sensitivity, as revealed via electrophysiology, shows a cosine function describing receptor firing intensity: accuracy depends on receptor orientation and arrangement and intensity-difference threshold.<ref name="Hoin-Radkovsky et al., 1984" />

In 2011 it was shown that there are certain fleshy ridges around each neuromast that direct water flow. When these ridges were removed, the receptive field for each neuromast was much wider than that with intact ridges; this was shown with electrophysiology.<ref name="Schwarz et al., 2011" /> The same experiment also showed that adding ridges to neuromasts that did not previously have ridges also altered the receptive fields for those neuromasts.<ref name="Schwarz et al., 2011" /> This suggests that local water flow is important in direction detection.

''A lineatus'' and other surface wave detecting fish have a limited range in which they can detect surface waves. The ratio of source distance/swim distance ranges between 0.84 and 1.20, and the means range from 0.98 to 1.07.<ref name="Hoin-Radkovsky et al., 1984" /> This translates to an accuracy of 85% or higher when stimuli are 6–19&nbsp;cm from the fish, decreasing to 76% at 14&nbsp;cm.<ref name="Müller and Schwartz, 1982" /> As the wave source gets farther from a fish, the fish's ability to accurately determine distance decreases until it can no longer detect the waves.<ref name="Bleckmann, 1980" />

''A lineatus'' uses the shape of the waveform to determine distance by analyzing how much the waveform has changed since it was generated; this amount of change is extremely predictable and regular. The surface waveform has high frequencies near source, and lower frequencies farther away due to the dampening effect of the water surface; the amount of decrease diminishes with distance.<ref name="Bleckmann and Schwartz, 1982" /> ''A lineatus''' possible use of the wavefront's curvature can be excluded since fish are still able to judge the distance of a wave's source with only a single functioning neuromast when all others have been ablated.<ref name="Müller and Schwartz, 1982" /><ref name="Bleckmann and Schwartz, 1982" /> When presented with single-frequency or upward frequency-modulated waves, fish underestimate the distance of the wave source; this suggests the normal downward FM of capillary waves, which arises almost immediately in wave dispersion, is necessary for ''A lineatus'' to judge distance.<ref name="Hoin-Radkovsky et al., 1984" /> This was confirmed in 1982 by presenting fish with waves with an artificially generated waveform so that at 7&nbsp;cm the wave had the downward FM sweep of a wave 15&nbsp;cm away, and fish responded to these by swimming 15&nbsp;cm.<ref name="Bleckmann and Schwartz, 1982" />

''A lineatus'' and similar surface feeding fish (e.g. ''Pantadon bucholzi'') use a slightly modified [[lateral line]] organ called a neuromast to detect surface waves. ''A lineatus'' has 18 neuromasts (specialized vibration-sensitive lateral line organs) on the dorsal surface of the head of ''A lineatus''. These are organized into three groups by longitudinal position, and each group is bilaterally symmetric. The groups are, caudal to rostral: nasal/infraorbital (I), supraorbital (II), and supratemporal/post-orbital (III).<ref name="Schwartz, 1965" /><ref name="Hoin-Radkovsky et al., 1984" /><ref name="Bleckmann and Mohr, 1998">Bleckmann, H., and Mohr, C. (1998) "Electrophysiology of the Cephalic Lateral Line of the Surface-Feeding Fish Aplocheilus lineatus". ''Comparative Biochemistry and Physiology'' 119A(3):807-815</ref>

Each neuromast is a cluster of hair-cell bundles arranged in a line and numbering in the 10s to 100s. Each bundle of hair cells is covered in a gelatinous capulla which the capillary waves actually make contact with and in doing so cause afferent neurons to fire.<ref name="McHenry and van Netten, 2007">McHenry, M.J. and van·Netten, S.M. (2007) "The flexural stiffness of superficial neuromasts in the zebrafish (Danio rerio) lateral line". ''Journal of Experimental Biology'' 210:4244-4253, cited in Schwarz 2011</ref> Neuromasts are similar in structure to canal organs in the lateral line canal system: they are housed in sacs of connective tissue between the skull and skin, and are connected to the water and water surface via canals and canal pores.<ref name="Hoin-Radkovsky et al., 1984" /> Recent work has also revealed small ridges of tissue around each neuromast which direct water flow around it.<ref name="Schwarz et al., 2011" />

The neuroanatomy beyond the receptor level for surface wave-detecting neuromasts has been minimally investigated. In this regard what research has been done shows considerable variation between species; in A lineatus, these neuromasts are considered the supraorbital line, and are innervated by ramus opthalmicus superficialis.<ref name="Müller and Schwartz, 1982, cited in Coombs">Müller and Schwartz, 1982, cited in Coombs S., Görner P., and Münz H. eds. ''The Mechanosensory Lateral Line: Neurobiology and Evolution'' (New York: Springer-Verlag New York Inc., 1989), pp.501-524</ref> This tract results in collateral fibers that innervate the rostral boundary of the medial octavolateralis nucleus, the area in all teleosts where lateral line organs innervate.<ref name="McCormick, 1981">McCormick. C.A. (1982) "Central projections of lateral line and eight nerves in the bowfin, Amia calva". ''Journal of Comparative Physiology'' 197:1-15, cited in Coombs S., Görner P., and Münz H. eds. ''The Mechanosensory Lateral Line: Neurobiology and Evolution'' (New York: Springer-Verlag New York Inc., 1989), pp.501-524</ref> These afferents also go to the valvula cerebelli.<ref name="Blubaum">Blübaum-Gronau, E., and Münz, H. (1988) "Topologische Reprasentation primarer Afferenzen einzelner Seitenlinienabschnitte beim Schmetterlingsfisch Pantodon bucholzi". ''Verg Dtsch Zool Ges'' 80:268-269, cited in Coombs S., Görner P., and Münz H. eds. ''The Mechanosensory Lateral Line: Neurobiology and Evolution'' (New York: Springer-Verlag New York Inc., 1989), pp.501-524</ref>

In one of the few electrophysiology studies performed on ''A lineatus'', it was found that of all the primary afferents from neuromasts that they recorded, half phase-locked to wave stimuli.<ref name="Bleckmann and Mohr, 1998" /> These neurons had weaker ongoing activity than non-phase-locked neurons. With waves of decreasing amplitude, phase-locking also decreased. Phase-locking was best in the 40–70&nbsp;Hz range or in the 80–100&nbsp;Hz range. Within a neuromast different afferents phase-locked best to waves of different frequencies and amplitudes, and they found no correlation between a unit's dynamic amplitude range and its ability to phase lock. Analysis of data revealed that wave amplitude of waves was encoded in the degree of phase-locking and in the afferent's firing rate. Since this was the extent of the feature representation found, it was concluded that further analysis of waves must happen at higher levels in the nervous system.<ref name="Bleckmann and Mohr, 1998" />

==Amphibians==

The [[African clawed frog]] (''Xenopus laevis'') responds to surface waves. It is able to locate wave directions at least to within ± 5°<ref name="Elepfandt">Elepfandt, A., (1982). Accuracy of taxis response to water waves in the clawed toad (Xenopus laevis Daudin) with intact or with lesioned lateral line system. Journal of Comparative Physiology, 148: 535-545</ref> and they can localize and distinguish between two different water waves coming simultaneously from two insects in different directions.<ref>{{cite web|url=http://www.t35.ph.tum.de/research/xenopus.en.html|title=Prey localization through the lateral-line system.|author=van Hemmen, J.L.|access-date=May 4, 2013}}</ref> Xenopus has approximately 200 lateral-line organs located along the sides of its body, and also around its eyes, head and neck. It is claimed these are used to navigate and detect prey either striking the water or struggling<ref>{{cite web|url=http://physicsworld.com/cws/article/news/2003/oct/16/frogs-turn-to-physics|title=Frogs turn to physics|author=Dumé, B.|publisher=Physicsworld.com|year=2003|access-date=May 4, 2013}}</ref> but the role of these organs in surface wave detection is not entirely clear; Xenopus with all of their lateral line organs destroyed are still able to respond to surface waves in an oriented fashion. Compared to animals with an intact system they respond somewhat less accurately to [[anterior]] stimuli and much less accurately to stimuli from behind.<ref name="Elepfandt" /> Areas of the Xenopus brain responding to surface waves have been identified.<ref>Branoner, F., Zhivkov, Z., Ziehm, U. and Behrend, O., (2012). Central representation of spatial and temporal surface wave parameters in the African clawed frog. Journal of Comparative Physiology A, 198: 797-815</ref>

It has been speculated that both Xenopus and the European grassfrog use their seismic sensory capabilities to locate conspecifics in breeding ponds.<ref>Narins, P.M., (1990). Seismic communication in Anuran amphibians. Bioscience, 40: 268-274</ref>

==Arachnids==

[[Dolomedes]] spiders hunt by waiting at the edge of a pool or stream. They hold on to the shore with their back legs while the rest of their body lies on the water, with legs stretched out. When they detect the ripples from prey, they run across the surface to subdue it using their foremost legs, which are tipped with small claws; like other spiders they then inject venom with their hollow jaws to kill and digest the prey. They mainly eat insects, but some larger species are able to catch small [[fish]].<ref>Barbour, T. (1921). Spiders feeding on small cyprinodonts. Psyche, 28: 131–132.[http://psyche.entclub.org/pdf/28/28-131.pdf]</ref><ref>University of Arkansas Museum Arthropod Museum web page: [http://www.uark.edu/ua/arthmuse//dolomede.html dark fishing spider (''Dolomedes tenebrosus'').]</ref>

Females of the water spider ''[[Argyroneta]] aquatica'' build underwater "diving bell" webs which they fill with air and use for digesting prey, molting, mating and raising offspring. They live almost entirely within the bells, darting out to catch prey animals that touch the bell or the threads that anchor it.<ref>Schütz, D. and Taborsky, M., (2003). Adaptations to an aquatic life may be responsible for the reversed sexual size dimorphism in the water spider, ''Argyroneta aquatica''. Evolutionary Ecology Research, 5: 105–117 {{cite web |url=http://www.zoology.unibe.ch/behav/pdf_files/Schuetz_EvolEcolRes03.pdf |title=Archived copy |access-date=2008-12-16 |url-status=dead |archive-url=https://web.archive.org/web/20081216214632/http://www.zoology.unibe.ch/behav/pdf_files/Schuetz_EvolEcolRes03.pdf |archive-date=2008-12-16 }}</ref>

[[Image:Male Nursery Web Spider.jpg|thumb|right|A male shows the typical hunting stance of the fishing spider, ''[[Dolomedes minor]]'']]

*The genera of spiders [[Pirata (genus)|Pirata]] and [[Dolomedes]]<ref name="Hoin-Radkovsky et al., 1984" />

*Clawed toad [[Xenopus laevis]]<ref name="clawed toad">Goener 1976, cited in Bleckmann and Schwartz, 1982</ref>

*Whirligig beetle [[Gyrinus substriatus]]<ref name="whirligig">Rudolph 1967, cited in Bleckmann and Schwartz, 1982</ref>

*Water strider [[Gerris remigis]]<ref name="waterstrider">Murphey 1971, Wiese 1969, cited in Bleckmann and Schwartz, 1982</ref>

*Back swimmer [[Notonecta glauca]]<ref name="backswimmer">Marckl and Wiese 1969, cited in Bleckmann and Schwartz, 1982</ref>

==See also==

*[[Seismic communication]]

{{reflist|33em}}

{{Neuroethology}}

{{diversity of fish}}

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[[Category:Animal physiology]]