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First published online May 21, 2007
Journal of Experimental Biology 210, 1925-1934 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.000075
Sharks need the lateral line to locate odor sources: rheotaxis and eddy chemotaxis
Boston University Marine Program, Marine Biological Laboratory, 7 MBL Street, Woods Hole, MA 02543, USA
* Author for correspondence at present address: University of South Florida, Department of Biology, SCA 110, 4202 E. Fowler Ave, Tampa, FL 33620, USA (e-mail: jaynegardiner{at}alum.bu.edu)
Accepted 13 March 2007
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Key words: Mustelus canis, lateral line, olfaction, plume tracking, rheotaxis, chemotaxis
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; Sheldon,
1909; Sheldon,
1911; Parker and Sheldon,
1913; Parker,
1914). They can find food sources without visual cues, while
animals with their nostrils blocked show no interest in prey; blocking one
nostril causes turning behavior to the intact side [`circus movements'
(Sheldon, 1911)], suggesting
that these animals steer by comparing odor concentration bilaterally
[`chemotropotaxis' (Fraenkel and Gunn,
1940)]. When presented with an attractive odor stimulus, the lemon
shark Negaprion brevirostris, a pelagic species, swims upstream into
the strongest current, regardless of where the odor source was actually
located (Hodgson and Mathewson,
1971), suggesting that this species' reaction to an odor stimulus
is to swim in the mean up-current direction, a process referred to as
`chemically stimulated rheotaxis'. How they determine the up-current direction
was not studied. This response would presumably bring them in proximity of the
odor source where other senses, such as vision, would then allow the animal to
precisely pinpoint the source (Mathewson
and Hodgson, 1972). In contrast, the nurse shark Ginglymostoma
cirratum, a benthic species, moves up the odor corridor to the source
(Hodgson and Mathewson, 1971;
Mathewson and Hodgson, 1972),
suggesting that for this species, a chemical stimulus triggers true
concentration gradient searching (`chemo-klinotaxis'). However, these animals
are unable to precisely locate an odor source in stagnant water
(Kleerekoper et al., 1975),
suggesting that flowing water provides a directional vector for localization.
In none of these studies was the eddy fine structure of the odor dispersal
process characterized or even considered. However, the chemical and momentum
dispersal fields typically associated with odor sources in nature contain
spatial gradients (of diluting odor peaks and decaying vorticity eddies
respectively) that can provide information about the direction and distance to
the source.
Analysis of the fine structure of odor plumes guiding animal behavior
indicated that they consist of highly dynamic and intermittent patterns of
odor patches and filaments, caused by turbulent mixing
(Murliss and Jones, 1981;
Elkinton and Cardé,
1984; Atema, 1985;
Moore and Atema, 1991;
Webster, 2007). As the time-averaged concentration of these peaks converges
too slowly to be useful to an animal tracking an odor plume
(Elkinton and Cardé,
1984; Webster and Weissburg, 2001), it is unlikely that a shark
could locate an odor source based solely on mean concentration gradients as
previously implicated (Hodgson and
Mathewson, 1971; Mathewson and
Hodgson, 1972). However, the eddies of the turbulent wake left
behind by moving prey or by a dead food item lying in moving water are
flavored with the odor of the prey or food. In complete darkness, catfish
track the odorous vortex trail left behind live prey, relying heavily on their
lateral line (Pohlmann et al.,
2004). Simultaneous detection of these flavored eddies by chemo-
and mechanoreceptors could provide animals both with detailed information
about the chemical identity of the source and with directionality in the
decaying wake for tracking it to the source, a process referred to as eddy
chemotaxis (Atema, 1996). Many
animals have chemo- and mechanoreceptor senses located in close proximity and
one might predict that their input converges in the brain. In the crayfish
brain, chemo-mechano receptive coincidence detector cells have since been
described (Mellon, 2005).
In fish, the lateral line, in particular the superficial neuromast system,
has been shown to function in the detection of large-scale turbulence (much
larger than the animal), allowing animals to orient to the mean flow
(Montgomery et al., 1997;
Baker and Montgomery, 1999a).
While aquatic animals are also known to use vision to orient to currents
(Lyon, 1904;
Lyon, 1909;
Arnold, 1974), mean flow
detection by the lateral line plays an important role during the localization
of stationary odor sources in flowing water, particularly in the absence of
visual information. Fish can use rheotaxis triggered by an olfactory stimulus
to find the source of the odor (Baker et
al., 2002; Carton and
Montgomery, 2003). Other evidence suggests that specifically the
superficial neuromasts of the lateral line system may be involved in rheotaxis
behavior in shark species that face the current while resting on the bottom
(Peach and Marshall,
2000).
The lateral line, in particular the canal neuromast system, has been shown
to function in the detection of small-scale turbulence (smaller than the
animal), where in teleost fishes it makes a major contribution to feeding and
prey capture behaviors (Coombs et al.,
2001). Fish use their lateral line to locate stationary sources of
small-scale turbulence (Janssen et al.,
1995) and track wakes of moving prey
(Pohlmann et al., 2001;
Pohlmann et al., 2004). Within
the elasmobranchs, the short-tailed stingray Dasyatis brevicaudata
can locate water jets, similar to those produced by the bivalves in their diet
(Montgomery and Skipworth,
1997). Although it has been suggested that the lateral line could
play a role in prey detection in sharks
(Tester and Nelson, 1967), its
contribution to odor plume tracking and food source localization in sharks
remains unknown.
In this study we assess the role of the lateral line in conjunction with
olfaction in the localization of sources of small-scale odorous turbulence; in
addition, we evaluate the role of the lateral line and vision in orientation
to large-scale (`mean') flow and small-scale object detection. The smooth
dogfish Mustelus canis (Mitchell 1815), was chosen for this study as
it is a small, benthic shark, 150 cm maximum length, suitable for laboratory
flume testing. The food search behavior of this species has been well
described (Parker, 1922), as
has the anatomy of its lateral line
(Johnson, 1917) and olfactory
structures (Sheldon, 1909;
Northcutt, 1978). With a diet
consisting primarily of lobster, crabs, shrimp and small fish, these
opportunistic feeders attack mainly sick and injured prey
(Field, 1907;
Bigelow and Schroeder, 1953;
Rountree and Able, 1996;
Gelsleichter et al., 1999).
This species is commonly found in New England bays and shallow inshore waters
and, being primarily a crepuscular/nocturnal hunter, it has been described as
finding its prey chiefly by olfaction
(Sheldon, 1909;
Parker, 1922;
Bigelow and Schroeder,
1953).
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10 000 liter near-laminar flow
flume, with a working area of 8.0 mx2.0 m lengthxwidth and filled
to a depth of 45 cm (Fig. 1).
At the downstream end, a start box of 2.0 mx2.0 m was created by a
removable grid made of a plastic egg crate material. The mean current
velocity, measured visually with Rhodamine B dye in the cross sectional center
of the flume, was 3.5 cm s–1.
The odor source in all experiments was squid rinse, prepared by soaking 100
g wet mass of freshly thawed squid in 1 l of seawater at room temperature for
1 h. The seawater control source was seawater taken directly from the flume.
These stimuli were delivered through soft PVC tubing (3.16 mm i.d.) at a rate
of 0.4 ml s–1, controlled by a Gilson Minipuls 3 peristaltic
pump with a 2 channel pump head (Gilson, Inc., Middletown, WI, USA). A small
lead weight kept the tubing hanging straight down even after being pushed by
the sharks. The tubing of both channels was connected to a nozzle made of hard
PVC connectors (5 cm long, 5 mm i.d.) delivering a mean flow velocity of
2 cm s–1, or about half the velocity of the flume's mean
flow, directed into the bottom boundary layer, parallel to the mean flow of
the flume. The Reynolds number of the nozzle (Re=100) indicates mild
jet turbulence; the physical object of the nozzle itself (and the small
attached lead weight) created an additional, small turbulent wake. Both
sources of nozzle turbulence, momentum surplus (jet) and momentum deficit
(wake), respectively, made small local additions to the major uniform
turbulence of the flume boundary layer. Given these conditions, we considered
the nozzles to be `oozing' odor sources, i.e. delivering odor (or seawater)
but not greatly changing the turbulent flow of the flume. The two nozzles were
placed symmetrically, 62 cm from each other (center to center) and 1 m from
the upstream flume collimator. Major wake turbulence was created by placing a
brick (20 cmx9 cmx6 cm) across the mean flow, 15 cm downstream
from each nozzle (Fig. 1). The
spacing between the upstream barrier and the stimulus targets was chosen so as
to not restrict the turning behavior of the animals. Mustelus canis
demonstrates great flexibility and is capable of performing tight
snout-to-tail turns.
This arrangement resulted in two parallel turbulent wakes, one composed of seawater flavored with squid odor (i.e. the typical odor plume), the other unflavored seawater (control seawater plume). The odor side was alternated regularly to account for possible side bias. Prior to any experiments, these plumes were visualized and photographed with 0.1 g l–1 of Rhodamine B dye dissolved in ambient seawater. The plumes remained spatially separate along the entire length of the flume. In sum, the nozzles generated two oozing plumes with minor turbulent wakes, carried downstream by the mean flow of the water in the flume tank where the two bricks generated additional major turbulent wakes. This gave the sharks four targets to locate, referred to as: odor alone (the odor nozzle), odor/turbulence (the brick on the odor side), seawater alone (the seawater nozzle), and seawater/turbulence (the brick on the seawater side).
Behavioral procedures
Prior to each trial, a shark was placed in the flume and allowed to
acclimate for at least 30 min, then offered a small piece of squid to confirm
its feeding motivation. If the animal would not feed, it was rejected from the
experiment. If the food was accepted, the animal was then herded into the
start box where it was held for 5 min while the plumes were allowed to
establish. The downstream grid was then briefly lifted and replaced, allowing
the animal to enter the test arena; this started the trial. Each trial lasted
10 min, during which time a characteristic push with the tip of the snout or
bite on a target was scored as a strike. Other target contact, such as
brushing a brick or nozzle with a fin, the tail, or the side of the snout was
disregarded as accidental contact. We scored the following three measures for
analysis of behavior. (1) `Success rate' defined as the proportion of trials
in which at least one strike occurred on any of the four targets. (2) `Search
time' from the beginning of the trial to the first strike on any target. (3)
`Number of strikes' on each of the four targets. In order to assess the
feeding motivation of each animal at the conclusion of each trial, a small
piece of squid was again offered. If this was not consumed within 10 min, we
considered the animal to lack the proper motivation to track and the prior
trial was rejected.
Light conditions
During trials, the room was normally illuminated by two overhead rows of
fluorescent lights, referred to as the light condition; a Sony Digital
Handycam camcorder (Sony Corporation of America, New York, NY, USA) was used
to record in detail the activities of the animal in the horizontal plane near
the targets. To test for the effect of visual information, animals were
deprived of visual cues by conducting experiments under infrared light (IR),
which is outside the known range of absorption of the visual pigments of
teleost fishes (Dartnall,
1975), as well as that of many sharks whose absorption peaks at an
average of 500 nm (Gruber and Cohen,
1978). The retinal ganglion cells of smooth dogfish, M.
canis, demonstrate a peak response at 505 nm and four logs of attenuation
by 700 nm (Stell et al.,
1975). During these tests, the overhead fluorescent lights were
turned off, any point sources of light in the windowless room were blocked and
the upstream end of the flume illuminated with a Tracksys IR LED Illuminator
(Noldus Information Technology, Leesburg, VA, USA) with mean output at 880 nm.
A Cohu 2700 Series 
inch monochrome camera (Noldus Information
Technology) was used to film the animal's activities in the horizontal plane
at the upstream end; behavior was simultaneously recorded to VHS tape and
played on a monitor in an adjacent room for manual scoring of any strike
activities as described above. IR illumination is referred to as the dark
condition.
Streptomycin treatment
Streptomycin has been shown to lesion both the surface neuromasts and canal
neuromasts in teleosts (Wersall and Flock, 1964;
Kaus, 1987;
Montgomery et al., 1997). In
amphibians, treatment with this drug results in an increase in spontaneous
firing of the afferent nerves, which is linked to direct effects on the
membrane of the hair cell, and a large lag phase in the receptor potentials,
which may be caused by interference with the motion of the sensory hairs
(Kroese and van den Bercken,
1982). Streptomycin administered externally has been demonstrated
not to affect inner ear function, which is based on similar hair cells, unless
applied intralumenally (Matsuura et al.,
1971).
We used streptomycin to treat eight of the animals (six males and two
females). Each shark was held in a heavily aerated 10 mmol
l–1 solution of streptomycin sulfate salt
(Blaxter and Fuiman, 1987) for
3 h (Montgomery et al., 1997).
Based on the evidence in teleosts and amphibians, we refer to streptomycin
treated animals as lateral line lesioned. Since teleosts treated with this
drug return to normal behavior in 20–24 h
(Blaxter and Fuiman, 1987),
the sharks were placed in the flume immediately after treatment, allowed to
acclimate, then tested in the light and in the dark as described above. Since
treatment with high concentrations of streptomycin results in effects in
amphibians that are only partially reversible
(Kroese and van den Bercken,
1982), all streptomycin lesion trials were done after completing
untreated trials. The light condition was randomized during all trials.
To test for effects of the treatment procedure itself, all eight animals were subjected to a sham treatment prior to streptomycin treatment by holding them in heavily aerated seawater for 3 h, followed by immediate acclimation and testing in the light as described above. Streptomycin-treated animals were offered a piece of squid following the trial; they were given 10 min to locate and consume the food, as with the untreated animals. However, if they were unable to locate the food in the dark, the lights were turned on and they were allowed an additional 10 min of food search time. If the food was not consumed during these additional 10 min, the prior trial was rejected.
Experimental design and data analysis
As we are working with large and complex animals we made every effort to
use as few animals as the statistical results would allow. With a small sample
size, individual differences among animals can have a large impact on the
results. We thus compared each animal to itself, pre- and post-treatment, to
minimize the impacts of individual differences.
For each of the four experimental conditions (intact in the light; intact in the dark; lateral line lesioned in the light; lateral line lesioned in the dark) and the sham treatment, behavioral performance was assessed by examining the parameters `success rate', `search time' and `number of strikes' on the four targets to analyze plume preference and target preference within the odor plume. Given the sequential measures of behavior of individual animals, we used non-parametric Wilcoxon Sign-Rank tests (WSR; SAS Institute Inc. 1995, #4090) to compare the response of individuals in the four experimental conditions as well as the sham control condition. For each animal, we calculated the `total number of strikes' per 10-min trial summed for all four targets. We then calculated the difference between the number of strikes on targets on the odor side and the seawater side, and tested whether that difference was significantly different from zero using a Wilcoxon Sign Rank test (two-tailed) in the Program JMP (SAS Institute Inc. 1995, #4090). A random distribution across the two sides (zero difference) is expected if a fish does not express a preference for the odor side or is unable to detect a difference between them. Finally, we tested for preference between the two targets on the odor side using the same Wilcoxon analysis.
Since each animal was tested more than once under each experimental condition, the total number of strikes, search time, and target preference of the animals were examined using block-wise analysis by Cochran–Mantel–Haenszel Statistics in the program JMP.
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Lateral line lesioned
After streptomycin treatment the intact success rate (which was 100% in
both lighting conditions) decreased somewhat in the light (to 71%, WSR=3.0,
N=8, P=0.2) and significantly in the dark (to 31%, WSR=10.5,
N=8, P=0.03; Fig.
2A). After streptomycin treatment five of the eight animals were
also unable to locate the piece of food in the dark, but then successfully
picked it up in less than 2 min once the lights were turned on.
In the light, streptomycin treatment resulted in longer search time: 291±78 s compared to 70±10 s (WSR=–18.0, N=8, P=0.008; Fig. 2B). Search time increased even further in the dark, to 508±59 s; this is significantly different both from the intact condition (WSR=–18.0, N=8, P=0.008) and from the condition with lateral line lesion in the light (WSR=–14.0, N=8, P=0.01; Fig. 2B).
In the light, the six out of eight animals that successfully located targets in the upstream end, demonstrated a significant strike preference for the odor targets over the seawater targets (odor, 12±7 strikes; seawater, 0.6±0.3 strikes; WSR=10.5, N=6, P=0.03), but they did not discriminate between the source of odor/turbulence and the source of odor alone (odor/turbulence, 8±5 strikes; odor alone, 4±2 strikes; WSR=5.5, N=6, P=0.1; Fig. 3C). In the dark, few animals successfully located targets in the upstream end (N=3); these few did not show a significant preference for the odor or seawater side (odor, 12±4 strikes; seawater 7±4 strikes; WSR=3.0, N=3, P=0.2; Fig. 3D).
These results indicate that lesioning the lateral line has serious effects on success rate, search time, target localization and target discrimination, and that visual information partially mitigates some of these effects. Two of the lesioned animals did not locate any targets even in the light.
Sham treatment
Sham treatment did not affect success rate (all animals located and struck
the objects in the upstream end during every trial, WSR=0, N=8,
P=1) or search time (pre-treatment, 69±8 s; post-treatment
86±19 s, WSR=–6, N=8, P=0.4). Sham treated
individuals continued to demonstrate a robust preference for the odor targets
over the seawater targets (WSR=18.0, N=8, P=0.008) and for
the source of odorous turbulence over odor alone (WSR=17.0, N=8,
P=0.02). These preferences were not significantly different before
and after sham treatment (odor-seawater, before vs after, WSR=11,
N=8, P=0.06; odor/turbulence-odor alone before vs
after, WSR=10, N=8, P=0.1). These results indicate that the
subsequently observed lesion and lighting effects were not caused by the
handling procedures.
Effect of repeated trials
Since the animals were tested more than once in each experimental condition
and since lighting alone did not have a significant effect on the success
rate, target preferences, or search time when the lateral line was intact,
these parameters, along with the total number of strikes, were screened for
order effects across the trials with intact lateral line. Success rate was not
affected by increasing number of trials: all animals were successful in all
trials. Similarly, preference for the odor side over the seawater side was
unaffected by trial order: all animals preferred the odor side over the
seawater side in all trials. Preference for the odor/turbulence target over
the odor target was unaffected by increasing number of trials (block-wise
analysis by Cochran–Mantel–Haenszel Statistics, z=4.33,
d.f.=5, P=0.5) as was search time
(Cochran–Mantel–Haenszel Statistics, z=13.71, d.f.=16,
P=0.6). Only the number of strikes decreased with increasing numbers
of trials (Cochran–Mantel–Haenszel Statistics, z=42.78,
d.f.=25, P=0.01).
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General behavioral description and motivational state of the animals
In the light and intact, the sharks exhibited rather stereotyped search
behavior upon encountering food odor: they quickly turned upstream and swam
directly up the odor plume to its source; near the source they executed an
immediate and precisely directed strike from above upon one of the source
objects. This is similar to previous descriptions
(Parker, 1922). The majority
of the first strikes occurred on the source of odor/turbulence (96%). It could
be argued that this is because it is the first target encountered while
swimming up the odor plume. However, we examined not only the first strike,
but all strikes that occurred over a 10-min period. After the first strike, a
bout of tight circling and/or figure-eights was performed in the vicinity of
the odor source, accompanied by additional strikes. These strikes occurred on
both targets on the odor side and very rarely on a target on the seawater
side. In typical shark fashion (Hodgson
and Mathewson, 1971; Mathewson
and Hodgson, 1972), when no food was found, the animals swam back
downstream for some distance, ignoring both plumes, and then retraced the odor
plume as described above to execute another bout of strikes. This pattern was
often repeated several times. Given that there were several bouts over the
course of a 10-min trial in which the animals displayed a mix of strikes on
both targets on the odor side, we are confident that the greatest overall
number of strikes on the source of odor/turbulence reflects the animal's
greater interest in this target rather than a first encounter advantage. In
the dark, we could observe their behavior only in the IR-illuminated vicinity
of the source; however, the final approach to the source did not appear to be
different from that in the light. Apparently, intact animals do not need
vision for the final localization of the target to be struck and the preferred
target is the odor/turbulence source.
Lesioned animals, in the light, again displayed food search behaviors including tight circling and figure-eights, but they swam much closer to the bottom of the tank than when intact. In the dark, few lesioned animals located the source. These few did not display a direct final approach and strike from above, but rather appeared to run accidentally into one of the source objects. The behavior that followed appeared frantic and erratic, with the animals performing wider circles and random strikes with poor direction, on all four targets in turn. Most of the animals were unsuccessful in locating any target during the 10-min trial and either did not even enter within the IR illuminated target area of the tank, or did enter but turned back downstream before reaching the targets. One might argue that after treatment they lacked the proper motivation for finding food. However, these animals eagerly consumed a piece of squid immediately following the conclusion of each trial. We conclude that they were motivated to track the odor plume during the trial but were unable to locate its source within the allotted time.
The piece of squid presents a different odor dispersal field, oozing in the
boundary layer almost without any additional turbulence. Some lesioned animals
were capable of tracking and locating this piece of food in the dark,
presumably based on olfaction alone; however, most needed light and therefore
additional visual input to locate it. These observations provide further
support for the conclusion that dogfish can find food by odor alone, but that
the additional presence of source turbulence provides more `convincing'
information leading to repeated strikes on the odor/turbulence source. The
sense of taste is not likely to play an important role in food finding since
nose-blocked dogfish cannot find food
(Sheldon, 1911).
Non-specific effect of streptomycin treatment
The effects of streptomycin on the elasmobranch lateral line are thus far
unknown; however, our behavioral results are consistent with known lateral
line lesion effects in teleosts
(Montgomery et al., 1997;
Coombs et al., 2001).
Streptomycin has been shown to lesion both the surface neuromasts and canal
neuromasts in teleosts (Wersall and Flock, 1964;
Kaus, 1987;
Montgomery et al., 1997),
although its effects on the two lateral line subsystems have not yet been
specifically compared. Since the hair cells of the inner ear remain unaffected
unless the drug is applied intralumenally
(Kroese and van den Bercken,
1982), the drug exerts its effect through direct contact with hair
cells that are either exposed to the environment (surface neuromasts) or to
the liquid contained within the canals, which are connected to the external
environment via pores. The electrosensory system is related to the
lateral line; however, its receptor cells are buried deeply at the end of long
ampullae of Lorenzini and separated from the environment by the jelly, which
would likely protect them from the effects of streptomycin. More importantly,
since we did not employ electric targets in this study, we can infer that the
observed target preferences are based on the use of other sensory modalities.
It is well known that when the nares of M. canis are physically
blocked to prevent odor access to the nose, they do not display any feeding
behaviors, even in the presence of visible food items
(Sheldon, 1911). Our animals
successfully located and consumed small pieces of squid after streptomycin
treatment, confirming that the olfactory sense was not affected. Based on all
of this evidence, we are confident that we observed lateral line lesion
effects after streptomycin treatment and not deficits in other sense
organs.
Effect of repeated trials
Since the `lateral line intact' and `lateral line lesioned' trials occurred
sequentially, it is important to evaluate if the decrease in success rate
following streptomycin treatment could be an effect of repeated trials. This
appears not to be the case, since search time prior to the first strike and
target preferences did not change after several trials: these animals chased
the odor with the same enthusiasm every time they were exposed to it. This
suggests that they were not aware at the start of a trial that the odor plume
was not originating from an actual food source, or that they were so motivated
that they ignored any memories they may have formed in association with the
overall experimental setup. Their interest in the targets began to wane only
after striking the targets and receiving additional tactile (and in this case
possibly gustatory) information that indicated to them that the objects in the
upstream end were not food. Thus it is the frequency of returns to the targets
for additional bouts of striking that decreases following repeated trials and
not the initial interest in the setup or in a particular target. Additionally,
following streptomycin treatment, the light and dark trials were conducted at
random so the observed behavioral differences are due entirely to increased
sensory deprivation.
The interplay of senses in odor plume tracking
Odor stimulated rheotaxis
While rheotaxis implies orientation to water flow, we argue that both
hydrodynamic and visual flow fields can be used to orient upstream. Moths
primarily use the visual flow field for anemotaxis, the air equivalent of
rheotaxis (Mafra-Neto and Cardé,
1994; Vickers and Baker,
1994), while we demonstrate here that the sharks can use both but
rely more on the hydrodynamic flow field than on vision. Intact animals
clearly demonstrated the ability to orient to the mean flow of the flume and
to navigate in an upstream direction on the odor side. Since the animals could
perform this function successfully and efficiently under both light and dark
conditions (Fig. 2A,B), visual
information is not critical to this behavior. This is not unexpected, given
that M. canis is primarily a nocturnal hunter
(Bigelow and Schroeder, 1953).
It suggests a major role of olfaction to trigger the upstream swimming with
directional information provided by the lateral line, presumably the free
neuromasts (Montgomery et al.,
1997; Baker and Montgomery,
1999b). This part of the search is a classic example of
odor-stimulated rheotaxis (Hodgson and
Mathewson, 1971; Mathewson and
Hodgson, 1972).
Vision
Once the lateral line system was disabled, most of the individuals in this
study could still successfully orient to the mean flow and navigate to the
upstream end of the flume as long as there was visible light. Since success
rate did not drop significantly after lesion
(Fig. 2A), it suggests that
these animals compensated for the lack of lateral line information using the
visual flow field for directional information. The animals may see features of
the environment drift by as they and/or the features are moved by the mean
flow of the water. Orientation in this manner has been described in teleost
fish (Lyon, 1904;
Lyon, 1909). Needless to say,
such visual input would be absent in extreme darkness and in featureless
visual environments such as open ocean. However, since the search time
increased significantly (Fig.
2B), it suggests that for M. canis, using visual
orientation to the mean current is slower and less efficient than using
lateral line information. The 29% failure rate after lateral line lesion in
visible light, although not statistically significant with our sample size,
still suggests that not all animals were always able to use vision to navigate
upstream to the targets, at least within the 10 min window allowed in these
trials, and that some individuals were better than others at visual
navigation.
Olfaction alone
Intact animals, regardless of light, always successfully located a piece of
real food. This small piece of dead meat provides an almost pure odor source:
it oozes odor into the bottom boundary layer and, in contrast to live prey,
generates no electric, hydrodynamic or acoustic fields. Apparently, such pure
odor sources can be better located when there is no `distraction' from a
nearby turbulence source, as seen in their preference for the odor/turbulence
target.
In the dark, lesioned animals did not discriminate between any of the
targets or between the odor and seawater plumes. This suggests that the few
strike successes (31%) appear to be by chance, such that the animals, while
swimming in the flume and excited by the odor, happened to find the upstream
area where perhaps tactile information triggered strikes on any or all four
targets. Only three of the lesioned animals were able to locate the piece of
food in the dark, though several of them were observed to swim over the food
on the first pass or to miss the piece of food on the first strike. The other
five animals only located the food after the lights were turned on. These
results indicate that without vision and lateral line information, and despite
an olfactory flow field, M. canis cannot efficiently navigate in the
mean flow of the flume nor pinpoint a piece of food. Thus, contrary to earlier
suggestions (Hodgson and Mathewson,
1971; Mathewson and Hodgson,
1972), olfaction alone cannot support efficient orientation and
tracking.
Eddy chemotaxis
Intact animals, once near the four stimulus targets, were more attracted to
the major source of turbulence on the odor side than to the source of the odor
itself. These preferences did not change with light condition, indicating that
they were not visually attracted to the largest object on the odor side, but
to the turbulence that it generated. This suggests that they tracked the wake
of the brick (on the odor side) and used the source of this turbulence as the
most probable identifier for the source of odor and thus food. Since the
animals only rarely struck targets on the seawater side and did not
discriminate between the source of seawater/turbulence and seawater alone, it
would appear that turbulence by itself is not particularly interesting to this
species. This is reasonable, since the natural environment is full of
uninteresting wakes. While wakes provide good directional information, odor is
far more informative for the identity of the source
(Atema, 1985). Therefore,
information contained in an odor-flavored wake combines two desirable
features: identity and directionality. This is the basis for the `eddy
chemotaxis' idea (Atema, 1995;
Atema, 1996;
Atema, 1998).
With a disabled lateral line system, target preferences changed. In the
light, the animals still displayed a significant preference for the odor side
over the seawater side, but they no longer discriminated between the source of
odor/turbulence and the source of odor alone. This further supports the
conclusion that intact animals were interested in the turbulence generated by
the brick, rather than its size or visual appearance, as once this turbulence
could no longer be detected, they were equally interested in both targets on
the odor side. Tracking the odor plume rather than the seawater plume
indicates that lesioned sharks can still roughly locate the source of a
turbulent odorous wake using olfaction and vision. However, increased search
time shows that they lost plume-tracking efficiency and the loss of target
preference shows that they lost precision in target localization. The most
coherent interpretation is that lateral line lesion not only affected
orientation to the mean flow field but also to the turbulent fine structure of
the plume. The pattern of decaying eddies in an odor plume can provide
additional directional information and the detection of a stream of flavored
eddies could further increase tracking efficiency and target discrimination
and localization. As an animal approaches the source of a turbulent odor
plume, both the odor peaks (Moore and
Atema, 1991) and eddy velocity peaks (Webster, 2007) become
stronger and more distinct. The mean hydrodynamic flow field is probably
detected best by the superficial neuromast system of the lateral line, since
the major stimulus is a velocity-coupled drag on the neuromasts. This
corresponds to behavioral results in teleosts
(Montgomery et al., 1997;
Baker and Montgomery, 1999a).
The turbulence fine structure provides local pressure gradients that are
detected best by the canal neuromasts system, and behavioral results confirm
this link (Coombs et al.,
2001). For eddy chemotaxis animals would then be using a
combination of olfaction and the canal system. This distinction is not as
trivial as it may seem. Turbulent jets and wakes consist of many scales with
eddies ranging from much larger to much smaller than the animal. The existence
of two distinct lateral line systems in many fishes seems to indicate the
importance of filtering information in two different hydrodynamic band widths:
large-scale flow for general upstream orientation and small-scale eddies for
jet and wake tracking, including close-up target localization. Studying live
prey detection, Kanter and Coombs (Kanter
and Coombs, 2003) came to the same conclusion based on the
detection of mean flow and small scale turbulence from prey (or a vibrating
sphere). Olfaction is essential in that it allows the animal to identify the
character of the source and to determine if it is worthwhile pursuing. It
triggers the initial upstream orientation and the subsequent plume tracking
and source localization. In addition, the vestibular inertial detection system
could be involved in even larger scale motion detection.
Olfaction and electroreception
The use of turbulence to provide directional information in an odor field
bears some resemblance to the shark's use of electroreception to pinpoint the
location of living prey. Kalmijn (Kalmijn,
1982) used M. canis to test the use of electroreception
in nature confirming his earlier laboratory results with Scyliorhinus
canicula (Kalmijn, 1971),
an animal strikingly similar to M. canis in terms of anatomy and
feeding ecology. He attracted the sharks with an odor plume, the source of
which was located on the bottom of a shallow bay between two sets of
electrodes. Whenever a shark approached the source area, one or the other of
the electrical stimuli, made to resemble the electrical field of a breathing
flounder, was switched on. Inevitably the sharks would strike the active
electrodes, bypassing the nearby odor source. Only when the electric field was
off did the sharks strike the odor source. This behavior is adaptive since the
electric field, although detectable only over short distances, is highly
directional and exists only in the presence of the animal. In contrast, the
odor field is less directional and can linger after the prey has left.
Conclusion
To locate food M. canis uses a suite of sensory information
varying with the nature and distance of the food source. It detects the
presence of an interesting distant source by olfaction. It then orients to the
mean flow field using the superficial lateral line (odor-stimulated rheotaxis)
and, when available, vision. It tracks the trail of small-scale, odor-flavored
turbulence using olfaction and the canal lateral line (eddy chemotaxis), and
also pinpoints the source of the plume with lateral line canals and olfaction.
For live prey, particularly when no significant wake is present, it uses
electroreception to direct the final strike
(Kalmijn, 1971).
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Acknowledgments |
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