Slow-moving predatory gastropods track prey odors in fast and turbulent flow
1 School of Biology, Georgia Institute of Technology, Atlanta, GA
30332-0230, USA
2 Skidaway Institute of Oceanography, Savannah, GA 31411-1011,
USA
* Author for correspondence (e-mail: ferner{at}skio.peachnet.edu)
Accepted 13 December 2004
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Summary |
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Key words: boundary-layer flow, Busycon carica, chemosensation, foraging success, hydrodynamic, odor plume, predation, temporal integration, turbulence, velocity
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Introduction |
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Given that turbulent water flow is both a common feature of benthic
environments and a major determinant of odor plume structure, it is necessary
to test the importance of hydrodynamics for olfactory searching in a variety
of taxa to elucidate the general constraints that foraging animals experience
in nature. Gastropod molluscs offer an intriguing contrast to crustaceans in
that these slow-moving animals hunt for similar prey in similar habitats while
using an entirely different array of sensors and behavioral strategies.
Although investigators rarely examine the impact of water flow on olfactory
navigation, studies of gastropod chemosensation have been a productive area of
research for more than half of a century (reviewed by
Kohn, 1961;
Mackie and Grant, 1974
;
Kats and Dill, 1998
). This
rich research lineage has broadened our understanding of the mechanisms and
importance of chemosensation by gastropods, and the chemical identity of
feeding stimuli has been a common focus of investigation
(Sakata, 1989
) leading to
detailed studies of physiological responses
(Elliot and Susswein, 2002
). A
few researchers have considered how the strength and stability of water
currents affect the olfactory behavior of gastropods
(McQuinn et al., 1988
;
Lapointe and Sainte-Marie,
1992
; Rochette et al.,
1997
) and one recent study tested the effect of increased flow
velocity on predation (Powers and
Kittinger, 2002
). However, no studies to date have examined the
impact of turbulence on the chemosensory responses of gastropods.
Successful olfactory predation should depend upon an individual's ability
to detect chemical stimuli in the environment and to locate the source of prey
odors faster than competitors. Weissburg
(2000) proposed a theoretical
framework that predicts how animal characteristics, such as size and mobility,
might interact to dictate effective olfactory strategies. Body size is
inherently related to the spatial scale of chemical information available to
receiving organisms, in that larger animals may be capable of simultaneous
odor sampling at different locations across a plume whereas spatial sampling
by smaller individuals is more restricted. Highly mobile foragers seem to
employ a strategy that relies upon intermittent bursts of chemical information
in conjunction with spatial comparisons
(Weissburg et al., 2002a
).
This sensory approach emphasizes rapid search at the expense of fine-grained
sampling. Conversely, slower animals might benefit by sampling more
successfully in the temporal domain. Averaging odor concentrations at a single
location over time could allow a slow-moving forager to estimate accurately
its position within a plume or its degree of progress towards an odor source.
This sampling strategy does not require reaction to instantaneous
concentrations contained in discrete odor filaments and, thus, should avoid
the apparently detrimental homogenization of plume structure associated with
turbulent mixing. Within this context, marine gastropods possess relatively
low capacity for spatial sampling but high potential for temporal integration,
simply by virtue of their sluggish movement that provides numerous sequential
sampling opportunities at each point within an odor plume. We therefore
predict that these slow-moving predators can locate the source of dissolved
prey chemicals even when the fine-scale structure of the odor plume has been
eroded by turbulence.
In the present study, we examined the chemosensory behavior of predatory
gastropods to test the hypothesis that turbulent water flow does not impair
the odor-tracking ability of slow-moving benthic foragers. Knobbed whelks
(Busycon carica, Gmelin) are common marine gastropods that consume
bivalves, such as oysters, scallops and clams, along the eastern coast of the
United States (Magalhaes,
1948; Carriker,
1951
; Peterson,
1982
; Walker,
1988
). These predators forage on intertidal flats and creeks
fringed by oyster reefs, as well as in subtidal channels that experience
largely unidirectional flow (Li et al.,
2004
). We exposed knobbed whelks to prey chemicals under
controlled laboratory flows and evaluated their ability to locate the stimulus
source in different current velocities. We then introduced additional
turbulent mixing near the stimulus source to decouple the effects of velocity
and turbulence on the properties of downstream odor signals. Results from this
study offer strong predictions about the relevance of the boundary-layer flow
regime for trophic interactions in estuarine communities. In contrast to the
generally accepted notion that physical forces diminish the severity and
importance of benthic predation, we propose that some olfactory predators
could thrive in more vigorous flows and might actually benefit from the
turbulent mixing of prey odors.
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Materials and methods |
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Characterization of laboratory flows
We conducted odor-tracking experiments in controlled hydrodynamic
conditions generated in the SkIO flume facility. This oval-shaped racetrack
flume is composed of polyvinylchloride (PVC) and powered by a paddle-wheel
drive system capable of sustaining a wide range of flow velocities. The paddle
system completely fills one of two parallel channels (7.3 m long, 1 m wide and
0.75 m deep) and the opposite channel contains a clear PlexiglasTM
working area where all experimental manipulations and observations were
performed. The curved section upstream of the working area is vertically
divided by four parallel partitions followed by a honeycomb baffle designed to
dampen large eddies and cross-stream flows. The smooth bottom of the working
area was covered with a 1 cm layer of graded sand [diameter=803±144
µm (mean ±1 S.D.); N=250] to provide a more
realistic sediment surface for whelk activity. The flume was filled to a depth
of 25 cm with estuarine water (2230) that was filtered through
gravel, sand and 5 µm polypropylene filter bags (Aquatic Eco-Systems, Inc.,
Apopka, FL, USA) to remove incoming organisms and suspended sediments. A third
of the flume water (approximately 2200 l) was exchanged each night to remove
chemical compounds derived from odor solutions and to match water conditions
with the holding tanks in which test animals were acclimated prior to
experiments.
Hydrodynamic treatments consisted of unidirectional flow at four different
free-stream velocities (U=1.5, 5, 10 and 15 cm s1)
with bulk flow Reynolds number (Re=Ud/, where
d is water depth and
is kinematic viscosity) ranging from 3800
to 38,000. These flow speeds are representative of natural whelk habitats,
where velocity ranges from zero at slack water to as high as 30 cm
s1 during peak tidal flow (M.C.F. and M.J.W., unpublished).
Additional treatments contained one of two obstructions intended to alter odor
plume structure independent of changes in bulk flow speed. We tested
obstructions at only one flow speed as an initial examination of whelk
responses to enhanced mixing and the intermediate velocity (U=5 cm
s1) selected for these obstruction treatments provided a
substantial increase in boundary-layer turbulence that exceeded the level
associated with our fastest flow condition (see Results). The first
obstruction was one of the symmetric halves of a 1 m section of PVC pipe
(o.d.=4.8 cm) that was cut along its longitudinal axis, oriented perpendicular
to the mean flow direction and positioned 1 cm upstream of the delivery nozzle
with the open side facing downward to create a `bump treatment.' The second
obstruction was a 30 cmcylindrical section of PVC pipe (o.d.=4.8 cm) oriented
vertically and centered 1 cm upstream of the delivery nozzle. Based on an
estimate of the cylinder Reynolds number (where d is the cylinder
diameter) and previous examinations of fluid motion around circular cylinders
(e.g. Taneda, 1965
;
White, 1991
), we expected that
this `cylinder treatment' should shed unstable vortices and introduce meander
not present in unobstructed flows. The frequency (f) of vortex
shedding downstream of the cylinder was estimated to be 0.2 Hz, based on the
nondimensional Strouhal number (S=fd/U), which
remains roughly constant over a wide range of Re spanning our test
conditions (Kundu, 1990
).
The flume was operated for 20 min before beginning data collection to allow the flow to stabilize at each new treatment condition and dye visualization confirmed that the flow was smooth and that wall effects were negligible throughout the central region of the working area. We used an acoustic Doppler velocimeter (ADV) to collect high-resolution, three-dimensional-velocity data (±0.01 cm s1) at various heights above the sediment surface to characterize boundary layer structure and to compare the different flow treatments quantitatively. The ADV probe (SonTek/YSI 10 MHz ADVField; Sontek/YSI, Inc., San Diego, CA, USA) was positioned in the center of the flume on an adjustable mount oriented to the nominal horizontal flow axis (x-direction) and measurement height was adjusted with a vernier sliding scale (±0.25 mm). Velocity data were collected at a frequency of 10 Hz and instantaneous measurements were averaged over 4 min to obtain velocity means and variances at each height.
Velocity profiles from unobstructed flow treatments were compared with the
generalized Karman-Prandtl log-profile relationship used to describe the
logarithmic increase in velocity above a boundary:
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Characterization of odor-plume structure
To quantify variation in odor plumes associated with different flow
treatments, we used salt water as a proxy for prey chemicals and collected
conductivity data describing the temporal structure of downstream stimulus
concentrations. The flume was initially drained, rinsed and refilled with
fresh water (0) to provide a featureless background against which
salt-water filaments could be resolved. A neutrally buoyant salt solution
(50
) was prepared by mixing concentrated salt water with anhydrous
ethanol. Matching densities of the resulting salt solution and flume water
were confirmed with a standard hydrometer (Welch Scientific Co., Skokie, IL,
USA) and the solution then was introduced through a delivery nozzle at the
same position and injection rate used for odor-tracking experiments (see
below). Salt concentrations were measured with a microscale conductivity and
temperature instrument (Precision Measurement Engineering, MSCTI Model 125;
Precision Measurement Engineering, Inc., Carlsbad, CA, USA). This
four-electrode sensor has a spatial resolution of approximately 1 mm and
extends from the end of a thin aluminum shaft oriented upstream and aligned
parallel to the sediment surface. Data were collected at a single point 1.5 m
downstream from the stimulus source where test animals began searching and the
sensor was positioned 2.5 cm above the sediment surface because a typical
whelk extends its siphon at about this height. Electrical conductivity of
water passing between the electrodes resulted in voltage differences that were
measured at a frequency of 10 Hz, amplified and recorded using National
InstrumentsTM software (LabVIEWTM 6).
A calibration curve (050) confirmed the linear relationship
between salinity and voltage output across the expected range of salinities
(r2=0.991, N=5). Three replicate data sets (30 s
each) were collected to characterize diagnostic features of plume structure
for each flow treatment and background conductivity of the flume water was
recorded for 1 min as a control prior to beginning each subset of
measurements. Data were analyzed to determine the number and average
conductivity of stimulus peaks (filaments) detected by the sensor. Peaks were
identified as discrete excursions above a baseline value that equaled the mean
conductivity of the preceding control. Voltages were normalized by the
conductivity of the source solution to facilitate comparison with other
investigations.
Preparation and delivery of prey chemicals
We standardized preparation and delivery of prey chemicals to provide a
consistent stimulus for foraging whelks. Initial tests confirmed that whelks
exhibit feeding responses to mantle fluid from a variety of bivalves including
ribbed mussels, which were selected as the source of prey chemicals for these
experiments. Mussels were collected from Cabbage Island in Wassaw Sound,
transferred to holding tanks in the SkIO flume facility and held for up to 1
week prior to stimulus preparation. Mussels were frozen and thawed immediately
before being opened to avoid shattering the shell and to reduce the extent of
damage during tissue extraction. Approximately 4 l of stimulus solution were
prepared for each trial by soaking freshly thawed mussel tissue in filtered
estuarine water drawn directly from the flume. Prey tissues were soaked for 1
h at a concentration of 7.5 g of tissue per liter of water and solutions were
filtered through a 60 µm screen before reintroduction to the flume. Lower
concentrations (e.g. 1.5 g l1) or shorter soaking times
failed to elicit a sufficient number of tracking responses, whereas higher
concentrations (e.g. 15 g l1) would have introduced
excessive quantities of prey chemicals into the flume and required more
frequent exchanges of flume water.
Dissolved prey chemicals were injected into the flow using a gravity-driven
delivery system suspended above the flume and upstream of the working area.
The stimulus solution was recirculated through a 1.2 l tank fitted with a
standpipe to allow excess solution to drain into an overflow reservoir. This
arrangement maintained constant head pressure on a delivery tube (Tygon®
2275, i.d.=6.35 mm) that exited the tank and passed through a flow meter
(Gilmont® GF-2360; Barnant, Barrington, IL, USA). Solutions were released
in the center of the flume at a constant rate of 52 ml min1
through a small brass nozzle (i.d.=4.7 mm; o.d.=6.4 mm) modified with a
fairing to reduce flow disturbances. The bottom edge of the nozzle rested at a
height of 1 cm above the sand to permit sufficient downstream advection while
ensuring that odors were retained near the sediment surface where whelks could
encounter them. Injection rate was selected to be isokinetic with a
free-stream velocity of 5 cm s1 to reduce the mixing of
odors by minimizing shear between the stimulus solution and ambient flow.
Despite the benefits of isokinetic release, injection rate was not adjusted to
match the other velocity treatments (1.5, 10 and 15 cm s1)
so as to avoid varying the flux of odor solution presented to test animals.
Total flux of chemical attractants can be an important determinant of animal
responses (Zimmer et al.,
1999; Keller and Weissburg,
2004
) and, thus, adjusting injection rate to preserve isokinetic
release would have required extensive additional tests of the interactive
effects of stimulus flux and flow velocity. The jet Reynolds numbers based on
relative velocity and outlet diameter were less than 700 and dye visualization
around the nozzle indicated that mixing due to shear was minor in all flows,
suggesting that an intermediate injection rate (of 52 ml
min1) was reasonable for the purposes of our
experiments.
Experimental tests of odor-tracking behavior
Olfactory tracking experiments were conducted in groups of four to six
consecutive trials at a given flow speed. Velocity for each group was chosen
at random and trials to be run at 5 cm s1 then were randomly
assigned to the cylinder, bump or unobstructed treatment. Individual whelks
for each trial also were randomly selected to receive either odor solution or
flume water (control) as an experimental stimulus. The 1 cm layer of sand
covering the working area of the flume was vigorously mixed after each trial
to flush out porewater odors and to release chemicals adsorbed to sand grains.
As many as three groups of trials were run in the same day, but no more than 8
h of odor release were permitted before the flume water was partially
exchanged overnight.
A single whelk was transferred from its holding tank to a flow-through cage (30x21x17 cm) constructed of plastic grating and located 1.5 m directly downstream from the delivery nozzle. The upstream wall of the starting cage was lifted after an acclimation period of 10 min during which time the whelks were exposed to the stimulus plume, and whelks then were allotted up to 20 min to begin upstream movement followed by an additional 40 min to locate the stimulus source. Total allowable trial time was based on preliminary measurements of whelk movement speed, which was estimated to be as slow as 0.5 mm s1 during active upstream searching. Trials were terminated and scored as a failed track if the whelk: (1) did not leave the cage within 20 min; (2) reached the side walls of the flume outside the lateral extent of the odor plume; or (3) did not track successfully within 60 min after the cage grating was lifted. Trials were terminated and scored as a successful track if the whelk moved to within 10 cm of the odor source before halting upstream or lateral movement. Dye visualization revealed that waterborne chemicals impacted the shell at this close distance, accumulating around the animal's siphon, foot and cephalic tentacles. Although most successful whelks (74%) proceeded to make direct contact with the delivery nozzle, inundation with stimulus solution close to the nozzle sometimes caused an individual to begin persistent digging behavior, presumably in search of what it perceived to be nearby prey. Whelks rarely advanced toward the nozzle opening after this behavioral shift occurred and so further observations were uninformative. All whelks that failed to locate the source of treatment or control plumes were offered a freshly killed mussel to confirm an adequate level of feeding motivation. Most unsuccessful whelks (62%) readily consumed the offered food, but those that did not begin ingestion within 2 h were judged to be uninterested in foraging and were excluded from subsequent analysis. The influence of flow velocity and obstruction treatments on the proportion of animals that tracked successfully was evaluated using a G-test for heterogeneity. Analysis of variance (ANOVA) was used to evaluate the effect of flow treatments on the total search time required for whelks to locate the stimulus source.
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Results |
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Profiles of turbulence intensity at the location of the delivery nozzle illustrated the effect of flow obstructions (Fig. 2A). The bump treatment increased turbulence intensity by a factor of 2.5 relative to the unobstructed or smooth condition, whereas turbulence in the overlying water column was unaffected or even slightly diminished, possibly due to flow impedance by the bump that extended across the entire width of the flume. The cylinder treatment disrupted flow at all depths and at the height of stimulus injection it increased turbulence intensity by more than four times relative to the smooth condition and nearly twice the level generated by the bump treatment. Downstream profiles of turbulence intensity confirmed that the hydrodynamic effects of obstructions persisted throughout the entire length of the test section (Fig. 2B). At the starting location of test animals, the bump treatment yielded a 50% greater level of turbulence than the smooth condition, whereas the cylinder treatment produced a threefold increase in turbulence intensity. Although we maintained the same free-stream velocity of 5 cm s1 across these treatments, the data in Fig. 2 demonstrate that, relative to the smooth condition, both obstructions increased turbulent mixing in the near-bed region where prey chemicals were introduced and delivered to foraging whelks. Moreover, these increases in turbulence exceeded those present in even the fastest unobstructed flows (see Fig. 1).
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Stimulus properties
Conductivity data revealed distinct patterns of chemical signal structure
associated with the various flow treatments. The slowest condition (1.5 cm
s1) was not included in this characterization because
accumulation of the salt solution hindered performance of the conductivity
sensor and prevented reliable measurements of concentration changes over time.
Differences in the number of stimulus peaks detected per second at the
downstream limit of the test section confirmed that the greater shear
associated with faster flow broke apart odor filaments and created more
numerous peaks (Fig. 3A), with
0.5 peaks per second detected in flows of 5 cm s1, compared
with 0.9 peaks per second in the fastest flows of 15 cm s1.
Greater numbers of peaks were accompanied by a concordant decrease in
concentration (Fig. 3A) because
the stimulus injection rate was constant across treatments. Average peak
concentration never exceeded 1.3% of the source concentration in any of the
conditions that we characterized, indicating that substantial dilution
occurred during stimulus transport. Taken together, these results demonstrate
that an increase in velocity alone disrupted odor signals in a manner
consistent with previous investigations (e.g.
Moore et al., 1994;
Finelli, 2000
).
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Obstruction treatments were designed to enhance mixing and homogenize stimulus concentrations similar to that in faster flows but without the associated effects of higher velocity (e.g. increased drag on foraging whelks). Conductivity measurements downstream of the bump and cylinder treatments showed an expected increase in the number of peaks detected per second and a decrease in average peak concentration (Fig. 3B). Compared with the 0.5 odor peaks detected per second in the smooth condition (Fig. 3A,B), the bump treatment generated 1.3 peaks per second and the cylinder treatment 1.7 peaks per second. In addition, turbulence generated by both obstructions incorporated `clean' water into the stimulus plume and diluted average peak concentrations even below levels observed in the fastest unobstructed flows (see Fig. 3A).
Tracking success
A total of 259 knobbed whelks were tested during the course of this study
and 179 of these individuals satisfied the post-trial criteria for feeding
motivation. Considering only those motivated foragers exposed to the odor
stimulus (N=102), between 3663% of whelks tracked successfully
in all six treatments (Fig. 4).
Tracking success was independent of flow speed (d.f.=3, G=2.46,
P>0.25), confirming that whelks were able to detect and follow
turbulent odor plumes equally well in flows ranging from 1.5 to 15 cm
s1. The apparent increase in tracking success at 5 cm
s1 (Fig. 4A),
although not statistically significant, could coincide with an optimal range
of velocity in which knobbed whelks are particularly successful at navigating
over smooth sand. At least 36% of test animals also located the odor source
when either one of the obstructions was present. Comparison of success rates
between obstructed and unobstructed conditions confirmed that whelk tracking
ability was independent of flow treatment (d.f.=2, G=2.55,
P>0.25), although the bump obstruction slightly reduced the
success rate of motivated searchers when compared with the cylinder treatment
or smooth condition (Fig.
4B).
|
Directed upstream movement was not simply a response to unidirectional flow or to disturbances associated with stimulus injection; no test animals in any flow treatment tracked to the delivery nozzle during control trials when unscented flume water served as a potential stimulus. Of the motivated foragers exposed to odorless control plumes (N=77), 43% showed no signs of activity and 38% exhibited a short period of digging followed by apparent inactivity. Only the remaining 19% left the starting cage and traveled to the edge of the test section or turned to move in a downstream direction, in contrast with the 68% of motivated foragers that actively left the starting cage when exposed to prey odors.
Successful searchers moved upstream while casting back and forth with their
siphon, apparently to maintain or confirm their continued presence within the
attractive odor plume (e.g. Fig.
5). Despite these casting motions, overall paths to the stimulus
source were rather direct, particularly in comparison to behavior displayed by
blue crabs searching in similar flows
(Weissburg and Zimmer-Faust,
1994). Comparison of mean search times across flow treatments
(Fig. 6) showed that successful
whelks reached the stimulus source more quickly in both faster (d.f.=3,
F=3.35, P=0.036) and more turbulent flows (d.f.=2,
F=3.77, P=0.049). Single degree of freedom post-hoc
tests revealed that search times in the two fastest treatments were
significantly shorter than in flows of 1.5 cm s1 and search
times in the cylinder treatment were significantly shorter than in
unobstructed flows of the same free-stream velocity. These increases in search
efficiency can be explained by the observation that cross-stream meandering
decreased in faster and more turbulent flows, and a more detailed kinematic
analysis of whelk search behavior is in progress (M.C.F. and M.J.W.,
unpublished).
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Discussion |
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According to Weissburg and Zimmer-Faust
(1993), reduction of crab
tracking success in more turbulent flows may be due to erosion of the viscous
sublayer or homogenization of odor plume structure, both of which reduce the
presence and intensity of discrete, concentrated odor filaments that blue
crabs use to locate a stimulus source. In comparison, a relatively large
proportion of whelks appear to overcome or even benefit from these same
disturbances. One explanation for whelk tracking success depends upon their
potential for collecting a temporal average of chemical concentrations.
Integrative sampling over a sufficient period of time would facilitate
detection of dilute odors or estimation of the mean concentration of a rapidly
fluctuating signal. This strategy should allow foragers to track chemical
signals that have been modified by mixing due to shear and turbulent
diffusion, particularly for slow animals such as whelks that have a limited
capacity for spatial sampling. As opposed to the discrete and concentrated
odor filaments that help to guide fast-moving blue crabs, a more continuous
signal of lower concentration may be suitable for whelks that are predisposed
for temporal integration. This notion is strengthened by the observation that
whelks tracked more efficiently when prey chemicals were disrupted by a
cylindrical obstruction. A recent study of blue crab responses to pulsed odor
plumes has shown that periodic odor release (on for 1 s, off for 4 s) degrades
both tracking success and search kinematics of blue crabs
(Keller and Weissburg, 2004
).
This time course of stimulus release is similar to the 0.2 Hz signal
modulation predicted from the Strouhal number for our cylinder treatment,
further indicating that search strategies are different and that whelks are
integrating over a longer period.
The persistent tracking ability of knobbed whelks also could relate to
their intrinsic capacity for stimulus detection across the
sedimentwater interface. These gastropod molluscs use their muscular
foot to push through sediments, glide over obstacles and envelop and consume
bivalve prey. Gastropod foot tissue is sensitive to a large number of
stimulatory chemicals and mixtures
(Nielsen, 1975;
Harvey et al., 1987
;
Dix and Hamilton, 1993
) and the
presence of prey chemicals within the matrix of sediment grains and porewater
should play a critical role in informing whelks of the quality, quantity, or
proximity of potential food resources. Both unidirectional flow and
bed-generated turbulence facilitate advective exchange of solutes across the
sedimentwater interface (Huettel
and Webster, 2001
), potentially enriching the stimulus environment
surrounding whelks. Subsequent adsorption to sediment grains or incomplete
flushing of porewater could retain attractive odors within the range of whelk
perception, and the ability to detect and respond to chemicals in this region
should enhance whelk navigational abilities in areas where waterborne cues are
less accessible. We thoroughly mixed sediments in the flume before and after
each trial to remove any chemicals that had become entrained, but future
experiments could be designed to tease apart the relative importance of
dissolved versus adsorbed cues for animal navigation.
The benefits of living in unconsolidated sediments are not restricted to
chemosensory processes. Vertical movement within mud or sand provides animals
with an option for refuge from adverse physical conditions as well as from
predation. Knobbed whelks must dig downward when pursuing infaunal prey and
often are found partially or completely buried within natural intertidal
sediments. In our flume experiments, whelks routinely displayed digging and
plowing behaviors rather than merely gliding across the sediment surface. This
partially submerged movement should allow whelks to maintain their body
position lower in the sediments to reduce the drag imposed on their shell, a
physical constraint that has clear ramifications for foraging blue crabs
(Weissburg et al., 2003). It
was difficult to interpret these behaviors, however, because we provided only
a 1 cm layer of sand for animals to move through. Previous experiments with a
smaller deposit-feeding gastropod indicate that burial is a common response to
rapid flow velocities (Levinton et al.,
1995
) and future studies using deeper sediments could clarify the
importance of whelk burial and subsurface movement within the context of
chemically mediated predation.
Importantly, knobbed whelks sometimes leave soft sediments to forage on the
harder surfaces associated with intertidal oyster reefs where the benefits of
burrowing ability are reduced (M.C.F., unpublished). The relative advantages
of hunting on shell substrates still need to be evaluated, although it is
unlikely that individuals remain on the same reef over multiple tidal cycles.
Oyster reefs along coastal Georgia are restricted to the middle intertidal
zone (Bahr, 1976) and whelks
that move onto an inundated reef are quickly exposed as the tide recedes.
Particularly during daylight hours in summer months, this exposure provides
incentive for whelks to retreat into deeper water or softer sediments where
they can bury themselves to avoid dessication and thermal stress. Surveys of
our collection sites over four successive low tides in August 2003 revealed
that whelks were visibly foraging on clams and oysters at night, whereas no
individuals were found exposed during daylight (M.C.F., unpublished). It is,
therefore, reasonable to assume that a substantial proportion of whelk
foraging effort is dedicated to navigating through soft sediments during the
approach to and departure from oyster reef habitats. If turbulent mixing of
prey odors is indeed beneficial to foraging whelks, then water flow over
oysters and other shell substrates could play an important role in guiding
whelks to profitable foraging areas.
The notion that physical forces can weaken the importance of predation has
aided the development of theories about factors that regulate community
structure. Connell (1975) and
Menge and Sutherland (1976
)
predicted that the relative importance of predation should decrease as the
foraging ability of consumers is suppressed along a gradient of increasing
environmental harshness. This concept of physical stress affecting the
strength of trophic interactions led to some interesting research (e.g.
Menge, 1978
;
Power et al., 1988
;
Peckarsky et al., 1990
;
Hart, 1992
;
Rilov et al., 2004
) and has
proven to be especially productive in studies of marine rocky intertidal
habitats (Menge, 2000
). For
example, comparison of benthic community dynamics between different flow
regimes in a Maine estuary showed that crab predation was most important in
low-flow sites, whereas recruitment and particle delivery dominated the
high-flow sites (Leonard et al.,
1998
). In contrast with the knobbed whelks that we investigated,
predators that live and forage primarily on hard surfaces do not have the
option for vertical retreat and therefore are faced with a different suite of
challenges in the search for prey and the tolerance of hydrodynamic forces.
Mobile predators in high-energy environments risk dislodgement due to wave
action and the drag associated with persistent exposure to rapid flow.
Furthermore, the vigorous and often violent hydrodynamic forces in rocky
habitats should quickly disperse dissolved prey chemicals, thus limiting the
spatial extent of olfactory navigation.
Compared with rocky intertidal habitats, less attention has been given to
the regulatory role of hydrodynamic forces within soft-sediment communities,
perhaps in part due to the difficult task of quantifying the spatial and
temporal distributions of resident organisms. The importance of boundary layer
flow is acknowledged in processes such as larval settlement
(Butman et al., 1988),
suspension and filter-feeding (Wildish and
Kristmanson, 1993
), sediment transport
(Hill and McCave, 2001
) and
biogeochemical cycling (Boudreau,
2001
), but only a few studies have directly investigated the
impact of hydrodynamics on predatorprey interactions in sedimentary
environments (e.g. Rochette et al.,
1994
; Finelli et al.,
2000
). Powers and Kittinger
(2002
) modified current
velocity on an intertidal sand flat and found that faster flow suppressed
foraging by blue crabs but had no apparent effect on the ability of knobbed
whelks to locate and consume hard clams. Interestingly, whelk predation on
scallops was enhanced in the high-velocity condition, suggesting that faster
flow either facilitated whelk behavior or impaired the ability of scallops to
detect and respond to approaching predators. Although Powers and Kittinger
(2002
) did not explicitly
consider the role of turbulence in their study, recent evidence from
laboratory experiments confirms that turbulent mixing alters the perceptual
abilities of hard clams in ways that affect their susceptibility to predation
(D. L. Smee and M.J.W., unpublished). Particularly in areas where regular flow
patterns are established, such as estuarine tidal channels, sedimentary
habitats that routinely experience more turbulent flows may provide a refuge
for some animals and a foraging opportunity for others. Field studies that
decouple the effects of turbulent mixing and advection should help to clarify
the importance of hydrodynamic forces for trophic interactions within these
benthic habitats.
In general, the effectiveness of sensory or navigational strategies may have significant impacts on competitive interactions. Odor-tracking abilities largely determine olfactory search success within a specified chemical and physical environment, and hydrodynamic forces that disrupt chemical signals may provide an underappreciated mechanism for resource partitioning among consumers that differ in their chemosensory potential. For example, fast-moving crustaceans should benefit from their rapid behavioral responses and locate odorous food more quickly than gastropods where flow velocity and shear are low. Conversely, sensory strategies employed by fast animals may limit their performance in turbulent conditions where stimulus plumes are homogenized. Slower predators therefore might have an advantage in turbulent flows due to their ability to continue pursuing prey in areas where odors are rapidly mixed and diluted. Our observation that whelks track prey odors successfully in flows that inhibit olfactory searching by blue crabs suggests the need to refine generalizations about how physical factors affect trophic interactions within benthic communities. The impact of hydrodynamic variability on chemosensory interactions could mediate patterns of organism distribution and abundance, but more realistic field investigations are needed to assess the ecological implications of flow variation and its interaction with animals of different sensory capabilities.
List of symbols and abbreviations
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Atema, J. (1985). Chemoreception in the sea: adaptations of chemoreceptors and behavior to aquatic stimulus conditions. Soc. Exp. Biol. Symp. 39,387 -423.
Bahr, L. M. (1976). Energetic aspects of the intertidal oyster reef community at Sapelo Island, Georgia (USA). Ecology 57,121 -131.
Boudreau, B. P. (2001). Solute transport above the sedimentwater interface. In The Benthic Boundary Layer: Transport Processes and Biogeochemistry (ed. B. P. Boudreau and B. B. Jorgensen), pp. 104-126. New York: Oxford University Press.
Butman, C. A., Grassle, J. P. and Webb, C. M. (1988). Substrate choices made by marine larvae settling in still water and in a flume flow. Nature 333,771 -773.[CrossRef]
Carriker, M. R. (1951). Observations on the penetration of tightly closing bivalves by Busycon and other predators. Ecology 32,73 -83.
Connell, J. H. (1975). Some mechanisms producing structure in natural communities: a model and evidence from field experiments. In Ecology and Evolution of Communities (ed. M. L. Cody and J. M. Diamond), pp. 460-490. Cambridge, UK: Belknap Press.
Crimaldi, J. P. and Koseff, J. R. (2001). High-resolution measurements of the spatial and temporal scalar structure of a turbulent plume. Exp. Fluids 31, 90-102.[CrossRef]
Derby, C. D. and Atema, J. (1988). Chemoreceptor cells in aquatic invertebrates: peripheral mechanisms of chemical signal processing in decapod crustaceans. In Sensory Biology of Aquatic Animals (ed. J. Atema, R. R. Fay, A. N. Popper and W. Tavolga), pp. 365-385. New York: Springer-Verlag.
Dix, T. L. and Hamilton, P. V. (1993). Chemically mediated escape behavior in the marsh periwinkle Littoraria irrorata Say. J. Exp. Mar. Biol. Ecol. 166,135 -149.[CrossRef]
Elliot, C. J. H. and Susswein, A. J. (2002).
Comparative neuroethology of feeding control in molluscs. J. Exp.
Biol. 205,877
-896.
Finelli, C. M. (2000). Velocity and concentration distributions in turbulent odor plumes in the presence of vegetation mimics: a flume study. Mar. Ecol. Prog. Ser. 207,297 -309.
Finelli, C. M., Hart, D. D. and Fonseca, D. M. (1999a). Evaluating the spatial resolution of an acoustic Doppler velocimeter and the consequences for measuring near-bed flows. Limnol. Oceanogr. 44,1793 -1801.
Finelli, C. M., Pentcheff, N. D., Zimmer-Faust, R. K. and Wethey, D. S. (1999b). Odor transport in turbulent flows: constraints on animal navigation. Limnol. Oceanogr. 44,1056 -1071.
Finelli, C. M., Pentcheff, N. D., Zimmer, R. K. and Wethey, D. S. (2000). Physical constraints on ecological processes: a field test of odor-mediated foraging. Ecology 81,784 -797.
Hart, D. D. (1992). Community organization in streams: the importance of species interactions, physical factors and chance. Oecologia 91,220 -228.[CrossRef]
Harvey, C., Garneau, F. X. and Himmelman, J. H. (1987). Chemodetection of the predatory seastar Leptasterias polaris by the whelk Buccinum undatum. Mar. Ecol. Prog. Ser. 40,79 -86.
Hill, P. S. and McCave, I. N. (2001). Suspended particle transport in benthic boundary layers. In The Benthic Boundary Layer: Transport Processes and Biogeochemistry (ed. B. P. Boudreau and B. B. Jorgensen), pp. 78-103. New York: Oxford University Press.
Huettel, M. and Webster, I. T. (2001). Porewater flow in permeable sediments. In The Benthic Boundary Layer: Transport Processes and Biogeochemistry (ed. B. P. Boudreau and B. B. Jorgensen), pp. 144-179. New York: Oxford University Press.
Kats, L. B. and Dill, L. M. (1998). The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience 5,361 -394.
Keller, T. A. and Weissburg, M. J. (2004).
Effects of odor flux and pulse rate on chemosensory tracking in turbulent odor
plumes by the blue crab, Callinectes sapidus. Biol.
Bull. 207,44
-55.
Keller, T. A., Tomba, A. M. and Moore, P. A. (2001). Orientation in complex chemical landscapes: spatial arrangement of chemical sources influences crayfish food-finding efficiency in artificial streams. Limnol. Oceanogr. 46,238 -247.
Koehl, M. A. R., Koseff, J. R., Crimaldi, J. P., McCay, M. G.,
Cooper, T., Wiley, M. B. and Moore, P. A. (2001). Lobster
sniffing: antennule design and hydrodynamic filtering of information in an
odor plume. Science 294,1948
-1951.
Kohn, A. J. (1961). Chemoreception in gastropod molluscs. Am. Zoologist 1, 291-308.
Kundu, P. K. (1990). Fluid Mechanics. San Diego: Academic Press.
Lapointe, V. and Sainte-Marie, B. (1992). Currents, predators and the aggregation of the gastropod Buccinum undatum around bait. Mar. Ecol. Prog. Ser. 85,245 -257.
Leonard, G. H., Levine, J. M., Schmidt, P. R. and Bertness, M. D. (1998). Flow-driven variation in intertidal community structure in a Maine estuary. Ecology 79,1395 -1411.
Levinton, J. S., Martinez, D. E., McCartney, M. M. and Judge, M. L. (1995). The effect of water flow on movement, burrowing and distributions of the gastropod Ilyanassa obsoleta in a tidal creek. Mar. Biol. 122,417 -424.[CrossRef]
Li, C., Blanton, J. and Chen, C. (2004). Mapping of tide and tidal flow fields along a tidal channel with vessel-based observations. J. Geophys. Res. 109, C04002, doi:10.1029/2003JC001992 .[CrossRef]
Mackie, A. M. and Grant, P. T. (1974). Interspecies and intraspecies communication by marine invertebrates. In Chemoreception in Marine Organisms (ed. P. T. Grant and A. M. Mackie), pp. 105-141. London, UK: Academic Press.
Magalhaes, H. (1948). An ecological study of snails of the genus Busycon at Beaufort, North Carolina. Ecol. Monogr. 18,377 -409.
McQuinn, I. H., Gendron, L. and Himmelman, J. H. (1988). Area of attraction and effective area fished by a whelk (Buccinum undatum) trap under variable conditions. Can. J. Fish. Aquat. Sci. 45,2054 -2060.
Menge, B. A. (1978). Predation intensity in a rocky intertidal community. Relation between predator foraging activity and environmental harshness. Oecologia. 34, 1-16.[CrossRef]
Menge, B. A. (2000). Top-down and bottom-up community regulation in marine rocky intertidal habitats. J. Exp. Mar. Biol. Ecol. 250,257 -289.[CrossRef][Medline]
Menge, B. A. and Sutherland, J. P. (1976). Species diversity gradients: synthesis of the roles of predation, competition and temporal heterogeneity. Am. Nat. 110,351 -369.[CrossRef]
Moore, P. A. and Atema, J. (1991). Spatial
information in the three-dimensional fine structure of an aquatic odor plume.
Biol. Bull. 181,408
-418.
Moore, P. A. and Grills, J. L. (1999). Chemical orientation to food by the crayfish Oronectes rusticus: influence of hydrodynamics. Anim. Behav. 58,953 -963.[CrossRef][Medline]
Moore, P. A., Weissburg, M. J., Parrish, J. M., Zimmer-Faust, R. K. and Gerhardt, G. A. (1994). Spatial distribution of odors in simulated benthic boundary layer flows. J. Chem. Ecol. 20,255 -279.
Nielsen, C. (1975). Observations on Buccinum undatum attacking bivalves and on prey responses with a short review on attack methods of other prosobranchs. Ophelia 13,87 -108.
Nowell, A. R. M. and Jumars, P. A. (1984). Flow environments of aquatic benthos. Annu. Rev. Ecol. Syst. 15,303 -328.[CrossRef]
Peckarsky, B. L., Horn, S. C. and Statzner, B. (1990). Stonefly predation along a hydraulic gradient: a field test of the harsh-benign hypothesis. Freshwater Biol. 24,181 -191.
Peterson, C. H. (1982). Clam predation by whelks (Busycon spp.): experimental tests of the importance of prey size, prey density and seagrass cover. Mar. Biol. 66,159 -170.[CrossRef]
Power, M. E., Stout, R. J., Cushing, C. E., Harper, P. P., Hauer, F. R., Matthews, W. J., Moyle, P. B., Statzner, B. and Wais De Badgen, I. R. (1988). Biotic and abiotic controls in river and stream communities. J. North. Am. Benthol. Soc. 7, 456-479.
Powers, S. P. and Kittinger, J. N. (2002). Hydrodynamic mediation of predator-prey interactions: differential patterns of prey susceptibility and predator success explained by variation in water flow. J. Exp. Mar. Biol. Ecol. 273,171 -187.[CrossRef]
Rilov, G., Benayahu, Y. and Gasith, A. (2004). Life on the edge: do biomechanical and behavioral adaptations to wave-exposure correlate with habitat partitioning in predatory whelks? Mar. Ecol. Prog. Ser. 282,193 -204.
Rochette, R., Hamel, J.-F. and Himmelman, J. H. (1994). Foraging strategy of the asteroid Leptasterias polaris: role of prey odors, current and feeding status. Mar. Ecol. Prog. Ser. 106,93 -100.
Rochette, R., Dill, L. M. and Himmelman, J. H. (1997). A field test of threat sensitivity in a marine gastropod. Anim. Behav. 54,1053 -1062.[CrossRef][Medline]
Sakata, K. (1989). Feeding attractants and stimulants for marine gastropods. Bioorgan. Mar. Chem. 3, 115-129.
Schlichting, H. (1987). Boundary Layer Theory. New York: McGraw-Hill.
Stachowicz, J. J. (2001). Chemical ecology of mobile benthic invertebrates: predators and prey, allies and competitors. In Marine Chemical Ecology (ed. J. B. McClintock and B. J. Baker), pp. 157-194. New York: CRC Press.
Taneda, S. (1965). Experimental investigation of vortex streets. J. Phys. Soc. Jap. 20,1714 -1721.
Walker, R. L. (1988). Observations on intertidal whelk (Busycon and Busycotypus) populations in Wassaw Sound, Georgia. J. Shell. Res. 7, 473-478.
Webster, D. R. and Weissburg, M. J. (2001). Chemosensory guidance cues in a turbulent odor plume. Limnol. Oceanogr. 46,1034 -1047.
Weissburg, M. J. (2000). The fluid dynamical
context of chemosensory behavior. Biol. Bull.
198,188
-202.
Weissburg, M. J. and Zimmer-Faust, R. K. (1993). Life and death in moving fluids: hydrodynamic effects on chemosensory mediated predation. Ecology 74,1428 -1443.
Weissburg, M. J. and Zimmer-Faust, R. K.
(1994). Odor plumes and how blue crabs use them to find prey.
J. Exp. Biol. 197,349
-375.
Weissburg, M. J., Dusenbery, D. B., Ishida, H., Janata, J., Keller, T., Roberts, P. J. W. and Webster, D. R. (2002a). A multidisciplinary study of spatial and temporal scales containing information in turbulent chemical plume tracking. Environ. Fluid Mech. 2,65 -94.[CrossRef]
Weissburg, M. J., Ferner, M. C., Pisut, D. P. and Smee, D. L. (2002b). Ecological consequences of chemically mediated prey perception. J. Chem. Ecol. 28,1933 -1970.
Weissburg, M. J., James, C. P., Smee, D. L. and Webster, D.
R. (2003). Fluid mechanics produces conflicting constraints
during olfactory navigation of blue crabs, Callinectes sapidus. J.
Exp. Biol. 206,171
-180.
White, F. M. (1991). Viscous Fluid Flow. New York: McGraw-Hill.
Wildish, D. J. and Kristmanson, D. D. (1993). Hydrodynamic control of bivalve filter feeders: a conceptual view. In Estuarine and Coastal Ecosystem Processes (ed. R. F. Dame), pp. 299-324. Berlin: Springer-Verlag.
Zimmer R. K., Commins, J. E. and Browne, K. A. (1999). Regulatory effects of environmental chemical signals on search behavior and foraging success. Ecology 80,1432 -1446.
Zimmer-Faust, R. K. (1989). The relationship between chemoreception and foraging behavior in crustaceans. Limnol. Oceanogr. 34,1367 -1374.
Zimmer-Faust, R. K., Finelli, C. M., Pentcheff, N. D. and
Wethey, D. S. (1995). Odor plumes and animal navigation in
turbulent water flow: a field study. Biol. Bull.
188,111
-116.