Two sniffing strategies in palinurid lobsters
Biology Department, Duke University, Durham, NC 27708, USA
* Present address: American Institute of Biological Sciences, 1444 Eye Street,
NW, Suite 200, Washington, DC 20005, USA
Author for correspondence at present address: University of California,
Department of Integrative Biology, Berkeley, CA 94720-3140, USA (e-mail:
patek{at}socrates.berkeley.edu)
Accepted 23 September 2002
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Summary |
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Key words: kinematics, olfaction, antennule, lobster, Palinuridae, chemoreception, Panulirus argus, Palinurus elephas, aesthetasc, leakiness, Reynolds number
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Introduction |
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Lobsters use their antennules to track the chemical signatures of food and
conspecifics (Fig. 1A;
Atema, 1995;
Atema and Voigt, 1995
;
Derby and Atema, 1988
;
Derby et al., 2001
;
Ratchford and Eggleston, 1998
;
Reeder and Ache, 1980
;
Zimmer-Faust et al., 1985
).
The lateral flagellum of the antennule has rows of specialized chemosensory
setae, the aesthetascs (Fig.
1B,C), in addition to other mechano- and chemosensory setae
(Cate and Derby, 2001
;
Grünert and Ache, 1988
;
Laverack, 1964
;
Steullet et al., 2002
).
Lobsters `sniff' by flicking the lateral flagellum through the water
(Moore et al., 1991a
;
Schmitt and Ache, 1979
);
during the fast closing phase, water flows through the chemosensory
aesthetascs, and during the slower opening phase, water is not replaced
(Goldman and Koehl, 2001
;
Koehl et al., 2001
). It has
been suggested that the generation of such intermittent flows by antennules
results in discrete sampling of the surrounding fluid
(Moore et al., 1991a
;
Schmitt and Ache, 1979
).
Indeed, Koehl et al. (2001
)
showed empirically that antennule flicking allows spiny lobsters to take
discrete samples of the temporal/spatial distribution of fine scale chemical
plumes in the environment.
|
Lobsters locate odor sources by using their antennules to sample an odor
plume's structure (Atema, 1996;
Moore and Atema, 1988
,
1991
;
Moore et al., 1991b
;
Zimmer-Faust et al., 1995
;
reviewed in Weissburg, 2000
;
Atema, 1995
). Within an odor
plume, small filaments with high odor concentrations spread from the odor
source. When crustaceans flick their antennules, they sample sharp
concentration gradients of the plume filaments. By tracking the spatial and
temporal distribution of these filaments in the environment, as well as other
environmental cues (e.g. current flow;
Zimmer-Faust et al., 1995
),
they can localize the source of an odor.
The chemical and fluid characteristics that are processed by an organism
are determined by the spacing of microscopic setae and a flagellum's speed
during a flick (Koehl, 1995);
these processes have been shown in both empirical and theoretical studies of
cylinder arrays (Cheer and Koehl,
1987a
,b
;
Hansen and Tiselius, 1992
;
Koehl, 1993
,
1995
,
1996
,
2000
;
Loudon et al., 1994
). In
general, when fluid flows across a surface, the velocity of the fluid in
contact with the surface is zero (no-slip condition); hence, a velocity
gradient, also known as a boundary layer, develops in the region adjacent to
the surface (Vogel, 1994
). For
a given geometry, the thickness of the boundary layer varies inversely with
Reynolds number (Re) a dimensionless parameter that describes
the relative magnitude of inertial and viscous fluid forces in a given flow
regime (Vogel, 1994
). Fast,
turbulent flows at large spatial scales are generally of high Re,
whereas slow, laminar flows at small spatial scales are generally of low
Re. The Re is defined as:
![]() | (1) |
The amount of fluid that passes through rather than around a lobster's
aesthetasc array is determined by the array's leakiness. In an array of
cylinders, when the boundary layers around two adjacent cylinders are large
relative to the distance between them, some proportion of the incident fluid
will be forced around rather than through the array. When the boundary layers
are relatively small, more fluid will leak through the array. Thus, the
leakiness of an array depends on (1) Re, which determines boundary
layer thickness, and (2) the relative size of the gaps between adjacent
cylinders, which is expressed as the ratio of the gap to the cylinder diameter
(Koehl, 1995,
2000
). Quantitatively,
leakiness is the volume of fluid that flows through the gap between cylinders
in an array divided by the volume of fluid that would flow through the same
area had the cylinders been absent (Cheer
and Koehl, 1987b
).
Across species, changes in velocity and setal spacing can modify the
transition point between leaky and non-leaky movements
(Koehl, 1995). In a copepod,
Centropages furcatus, the setae on the second maxillae are widely
spaced and typically function as a rake (capturing particles as water flows
through the structure). When maxillae velocity is decreased, the appendage
acts like a paddle (most of the particle-laden water flows around rather than
through the structure). By contrast, the copepod Temora stylifera,
has more closely spaced setae and the maxillae normally function as paddles,
but, when velocity is increased, the maxillae act as rakes. These different
strategies illuminate the importance of both morphological and behavioral
modifications for changing the fluid dynamics of sensory appendages across
species (Koehl, 1995
). An
organism that modifies the speed of its sensory appendage and/or the relative
size of the gaps between its sensory hairs can adjust the way it samples
chemical information in the environment.
Studies of chemoreception in aquatic crustaceans have focused on a broad
array of taxa, including spiny lobsters (Palinuridae:
Derby and Atema, 1988;
Grünert and Ache, 1988
;
Reeder and Ache, 1980
), clawed
lobsters (Nephropidae: Atema,
1995
; Atema and Voigt,
1995
), crayfish (Cambaridae:
Dunham et al., 1997
;
Moore and Grills, 1999
;
Oh and Dunham, 1991
) and crabs
(Portunidae: Weissburg and Zimmer-Faust,
1993
,
1994
). Most studies of lobster
chemoreception have focused on Panulirus argus (Palinuridae) and
Homarus americanus (Nephropidae), with few studies comparing species
within these families (Cate and Derby,
2002
), although some studies have compared these model species to
other crustaceans (e.g. Ghiradella et al.,
1968
; Laverack,
1985
).
In the present study, we compare Panulirus argus (Caribbean spiny lobster) to Palinurus elephas (common spiny lobster) to determine how major structural differences in chemoreceptor organs influence the capture of odor molecules from the environment and to assess the relevance of the P. argus model to other palinurid lobsters. (Note: these species are in different genera with similar names.) We describe the morphology and kinematics of the antennular flagella in P. elephas through the use of scanning electron microscopy, high-speed videography and a new method of digital video analysis. We compare Re and leakiness parameters to those previously described in P. argus and propose a functional interpretation for the two dramatically different strategies used by these species in acquiring chemical information. We measure antennule structures across all major genera in the Palinuridae and estimate the amount of water sampled by different antennule sizes. To our knowledge, this is the first time that the antennular kinematics of a palinurid species other than P. argus has been studied. Furthermore, this comparative study offers a first step towards understanding the behavioral function of the remarkable antennule variation across the palinurid family.
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Materials and methods |
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Microscopy and morphological descriptions
The microscopic anatomy of the flagella was examined using stereo light
microscopy and scanning electron microscopy (SEM). We removed the antennules
from freshly euthanized lobsters. The tissue was immediately placed in 2%
glutaraldehyde in phosphate-buffered saline and fixed for 1.5 h [see Dykstra
(1992)]. The tissue was rinsed
in distilled water and dehydrated in an ethanol series. The specimens were
stored in 100% ethanol until critical point drying and then were sputter
coated (60:40 gold:paladium mix, Anatech Hummer V, Anatech Ltd, Springfield,
VA, USA) and observed at up to 2500x magnification with a scanning
electron microscope (Philips 501 SEM, Oregon, USA). The lateral and medial
flagella were cut into four and two smaller sections, respectively, in order
to mount on stubs in the scanning electron microscope. The guard hairs were
removed in some samples in order to view the aesthetascs.
Aesthetasc diameter and the gap distance between rows of aesthetascs were measured from digital images captured from the SEM (Scion Image, v.4.0.2, Maryland, USA). Aesthetasc diameter and gap distance between each aesthetasc were measured at the base of the aesthetascs near their insertion on the flagellum. Average measurement error was 2.3% of the mean. We sampled ten aesthetascs and ten gaps from four individuals. Digital SEM images of a calibration disk (Ted Pella, Inc., Redding, CA, USA) were used for calibrating images of antennules.
Comparative antennule morphology
We measured lengths of the peduncle segments and flagella of 17 lobster
species using preserved specimens housed at the National Museum of Natural
History, Smithsonian Institution, Washington, DC, USA. Each major genus of the
Palinuridae was represented, as well as members of the Nephropidae
(Homarus americanus) and the Scyllaridae (Parribacus antarcticus,
Scyllarus arctus). Body size was approximated as carapace length (base of
the rostrum to the posterior margin of the carapace). Two specimens per
species were measured when possible.
High-speed videography
A high-speed video system (HR1000, Redlake Motionscope Systems, San Diego,
CA, USA) recorded images of the P. elephas antennules as they
flicked. The system's tripod-mounted camera recorded images of the two
flagella on each antennule. Images of antennule flicking in which the lateral
flagellum was perpendicular to the camera's lens were collected at 500 frames
s-1 and stored on SVHS videotape. Later, video fields were
digitized and stored as sequences of individual bitmap images (TIFF
format).
Motion analysis
We designed an automated method that does not rely on traditional motion
analysis techniques to track flagellum movement. Video images could not
resolve natural markings on the flagella and we were unable to use physical
markers because they either damaged the delicate antennules or were removed by
the animal. To circumvent these problems, we quantified the motion of the
antennule's lateral flagellum by tracking the intersection between the edge of
the flagellum and a line fixed in the image plane
(Fig. 2A). The line intersected
the distal end of the aesthetasc-bearing region of the flagellum and ran
tangent to the arc traced by a point on the flagellum when it moved. For the
small angular excursions subtended by the flagella during a flick
(approximately 5°), the maximum deviation between the tangent line and the
circular path of a point on the flagellum was approximately 0.1% of the
diameter and thus was neglected.
|
Image processing consisted of: (1) filtering, (2) sampling pixel intensity along the tangent line and (3) edge detection. First, an adaptive Wiener algorithm acted as a low-pass filter to reduce noise in the image [local means and standard deviations were calculated for each pixel using an area set at 5 pixel x 5 pixel window (Matlab v. 6, The Mathworks Inc., Natick, MA, USA)]. Second, a tangent line was drawn on the image for each flick sequence using a software graphical interface. Image-processing software sampled the intensity of each pixel along the line for each image in a sequence. Third, the edge was detected along the tangent line at locations where the intensity of the pixels changed from light (background) to dark (flagellum). We tracked the position of the intensity transition over the course of each flick (Fig. 2B).
We determined the position of the transition from background to flagellum by comparing the intensity difference between the end pixels of a 3-pixel wide window passed along the tangent line (Fig. 2). The position of the transition depended on a threshold value of intensity difference. Within a range of threshold values, our method detected the same edge but located it at slightly different positions. Outside of the threshold-value range, the method either detected an edge in the background (resulting from noise in the pixel intensity of the background) or did not detect an edge at all. Rather than choose a single threshold value arbitrarily, we determined a range of threshold values that properly detected all of the edges in a flick sequence and used the mean edge position determined over that range of threshold values. The standard deviation of edge position measurements over the range of threshold values never exceeded 3% of the mean.
To track the position of the flagellum over time we first filtered the raw
position data to remove high-frequency noise and then calculated the speed.
The filtering algorithm consisted of four steps: (1) filtering the data with a
second-order low-pass Butterworth filter, (2) reversing, with respect to time,
the output, (3) filtering with the same filter again and (4) reversing, with
respect to time, the output of the second filter
(Winter, 1990). Re-filtering
of the reversed data introduced a phase shift equal and opposite to that
introduced by the first filter, and thus the algorithm resulted in filtered
data in phase with the raw data. Residual analysis revealed that a cutoff
frequency of 100 Hz balanced the amount of noise passed through the filter
with the amount of signal distortion introduced by the filter
(Winter, 1990
). We applied a
numeric differentiation technique to calculate the speed of the flagellum. The
speed at a time point was estimated to be the distance moved by the flagellum
divided by the time increment between two video frames.
We converted kinematic measurements from pixel units to SI units by measuring the pixel dimensions of a known antennule structure in the image using Scion Image (the actual size previously was measured on the live specimens). Imprecision, expressed as the standard deviation of repeated measures of the same structure, was typically 5% of the mean within an image and 3% of the mean between different images within a time sequence.
Determination of Reynolds number
In assigning the variables used to calculate Re (equation 1), we
recognized that to an observer fixed in still fluid during a flick, the
flagellum's speed equals the freestream flow speed in the flagellum's
reference frame. Thus, we followed convention and chose U as either
the peak or mean speed of the lateral flagellum during each phase of a flick
(Goldman and Koehl, 2001;
Mead et al., 1999
). Because a
flicking flagellum rotates about a fixed point, the freestream flow, and thus
Re, will vary linearly along the flagellum's length. We report speeds
and Re values encountered at the distal end of the aesthetasc-bearing
region of the antennule. Aesthetasc diameter is used as the length scale
(L) to be consistent with both empirical studies of flow through
arrays of cylinders and studies of other biological sensors that bear
hair-like sensilla (Goldman and Koehl,
2001
; Hansen and Tiselius,
1992
; Koehl, 1993
,
1996
,
2000
;
Mead et al., 1999
). The
kinematic viscosity (
) of seawater (35
) at 10°C is
1.36x10-6 m2 s-1
(Sverdrup et al., 1942
;
Vogel, 1994
).
Statistics
We tested whether the following kinematics parameters varied between the
closing and opening phases of each flick: Re, maximum and average
flagellum speed, duration and distance moved (excursion). For duration
measurements, 26-39 flicks from each of four individuals were measured. For
all other kinematic measurements, 11-39 flicks from each of four individuals
were measured. Data were tested for normality using a ShapiroWilk test
(Zar, 1999). As the data did
not conform to a normal distribution, differences between flick phases across
individuals were tested using a nonparametric KruskalWallis test
(Zar, 1999
). Significance
level was set at P=0.01 to account for multiple comparisons
(Sokal and Rohlf, 1981
).
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Results |
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|
|
An array of plumose setae extends along the length of the medial flagellum (Fig. 3E,F). These setae extend ventro-laterally and remain ventral to the lateral flagellum during a flick (Fig. 4). An array of long, simple setae extends along the dorsal surface of the flagellum (Fig. 4). The long axis of the simple setae extends dorso-ventrally, whereas the plumose setae run perpendicular to the lateral flagellum's flick (Figs 3, 4).
|
Panulirus species have considerably longer flagella per body length than any other measured species, with the medial flagellum extending to up to three times the carapace length (Table 2; Fig. 5). The medial flagellum is longer than the lateral flagellum in all the species. The total peduncle length is relatively constant across taxa, although Justitia longimanus (West Indian furrow lobster) has a relatively high total peduncle length. Excepting Parribacus spp. and Scyllarus spp., the first segment of the peduncle is longer than the subsequent segments (Fig. 5; Table 2). The second and third segments of the peduncle are similar to each other in length. Lateral flagellum length varies dramatically across the lobsters (Fig. 6A). By contrast, most variation in total peduncle length appears to be explained by body size across taxa (Fig. 6B; Table 2).
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|
Kinematics and Reynolds number
The flick of the lateral flagellum of a P. elephas antennule is a
short reciprocal motion during which the flagellum executes a ventral
excursion (closing phase) followed by an immediate return to or near the
initiation point (opening phase) (Fig.
4). The medial flagellum is not actively moved during a flick but
it does flex slightly in passive response to the impulsive motion of the
lateral flagellum. Flicks were often executed in rapid succession with
interspersed periods of quiescence (Fig.
7).
|
We found significant differences between flick phases in all measured parameters except excursion distance (Table 3). Individuals differed significantly (P<<0.01, N=4) in all parameters except flick duration, so flick phase comparisons were calculated within each individual. Both the peak and the mean speed of the initial closing phase were approximately twice those of the opening phase of the flick (Fig. 7; Table 3). Furthermore, as the distance traveled by the flagellum was nearly equal in both phases of the flick, the duration of the flick phases also differed by a factor of approximately two (Fig. 7; Table 3). The Re of an aesthetasc during both phases of a flick is in the order of one. During the closing phase, the aesthetasc Re is approximately twice the aesthetasc Re during the opening phase (Table 3).
|
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Discussion |
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Flicking kinematics and morphology in Palinurus elephas
and Panulirus argus
P. elephas sniffs by flusing more water through the aesthetasc
array during the relatively rapid closing phase of each flick than during the
slower opening phase. By flicking its lateral flagella such that the
aesthetasc tuft operates at Re values of approximately one, the
leakiness of the aesthetasc array is sensitive to small changes in
Re. If the aesthetasc array operated in an Re range that was
an order of magnitude higher or lower, small Re changes would not
affect leakiness: at Re values of approximately one, small
differences in the speed of flick phases cause relatively dramatic differences
in the leakiness of the aesthetasc array. If we apply the leakiness estimates
generated by Hansen and Tiselius
(1992; pp. 826-827) to the
present study, we find that the leakiness of P. elephas aesthetasc
arrays averages approximately 0.40 (0.70 peak) during the closing phase and
0.25 (0.30 peak) during the opening phase of flicks. Hence, P.
elephas sniffs by varying the flagellum's speed between the two flick
phases, such that the closing phase is 60-130% more leaky than the opening
phase.
Considering that mammals, snakes and other crustaceans discretely sample
odors, it comes as no particular surprise that P. elephas also does
so. It is surprising, however, that none of the factors that determine
Re flow speed, aesthetasc diameter and kinematic viscosity
are the same in P. elephas and P. argus, yet the
mean Re of the closing phase is the same in each species and the mean
Re of the opening phase is remarkably similar
(Table 4). Both species operate
their antennules in the Re range where leakiness is sensitive to the
speed of the flick. If the flagella of P. elephas were merely
geometrically scaled up to be the same length as those of P. argus
and the angular velocity held constant, the relative spacing of the
aesthetascs would remain constant but the Re range would cause both
phases of the flick to be very leaky and the animal could not take discrete
odor samples. On the other hand, if the flagella of P. argus were
simply scaled down to the same length as P. elephas, neither flick
phase would allow much fluid to enter the aesthetasc array and diffusion would
move molecules from the fluid to the surface of the sensilla [although see
Trapido-Rosenthal et al.
(1987) for a discussion of
enzyme-mediated chemoreception at sensillar surfaces]. Thus, in spite of both
morphological and kinematic differences, P. elephas and P.
argus discretely sample the fluid by flushing it through their aesthetasc
arrays during the fast, leaky closing phase of a flick and retaining that
sample of fluid during the slower, less leaky opening phase
(Koehl, 2000
;
Goldman and Koehl, 2001
;
Koehl et al., 2001
).
|
Even though P. elephas and P. argus use the same
mechanism to discretely sample odors, the spatial and temporal characteristics
of the water samples are distinctly different. The duration of each flick
phase is nearly an order of magnitude lower in P. elephas than in
P. argus (Table 4),
hence the two species have vastly different flicking frequencies. P.
argus flick at a frequency between 0.4 Hz and 1.5 Hz and increase
flicking rates up to 3.5 Hz in the presence of food scent
(Gleeson et al., 1993;
Goldman and Koehl, 2001
). We
found that P. elephas flick at approximately 20 Hz; in one case this
rate was sustained for over 0.8 s. In addition, the lateral flagella of P.
argus are nearly seven times longer and the distal end of each flagellum
travels four to five times further during a flick than do the lateral flagella
of P. elephas (Tables
3,
4; Figs
5,
6).
Differences in the setae on the medial and lateral flagella also
distinguish P. elephas and P. argus. Non-aesthetasc setae
are important in acquiring mechanical and chemical information, complementary
to that acquired with the aesthetascs
(Steullet et al., 2001). On
the lateral flagellum, P. argus has simple companion setae, whereas
P. elephas and other palinurids have plumose companion setae (pc,
Fig. 3; Cate and Derby,
2001
,
2002
). The function of these
companion setae has yet to be determined, but the absence/loss of setules in
Panulirus species suggests a change in mechanical sensitivity through
modification of flow around the setae. On the medial flagellum, the plumose
setae of P. elephas appear as though they would influence flow into
the aesthetasc array during the closing phase of the flick
(Fig. 4), but, at these
Re values, motion near surfaces does not alter the leakiness of
cylinder arrays (Loudon et al.,
1994
). P. elephas lacks the peculiar zigzag orientation
of aesthetasc tips found in P. argus, which has been proposed to
channel fluid between neighboring aesthetascs and thereby facilitate diffusion
across the laminar region surrounding aesthetascs
(Fig. 1C;
Gleeson et al., 1993
;
Goldman and Koehl, 2001
). In
P. argus, fixation of the antennules can disrupt the zigzag
arrangement of the aesthetasc tips; thus, the clustering of aesthetasc tips
towards the center of rows in P. elephas may be an artifact of the
glutaraldehyde and alcohol tissue preservation applied to the flagella.
Antennule morphology across the Palinuridae
Both antennular flagellum length and total peduncle length vary across the
Palinuridae (Table 2; Figs
5,
6). Peduncle length is
relatively short in the nephropid lobsters, however most variability across
the palinurids can be explained by body size (Figs
5,
6). Antennular flagellum
length, by contrast, is highly variable across the palinurids.
While the peduncle length determines the maximum distance from the animal
at which water can be sampled, the flagellum length determines the amount of
water sampled per flick (proportional to the number of aesthetasc rows on the
tuft). In each species, we estimated the area of water sampled per degree of
movement () by the lateral flagellum as follows:
![]() | (2) |
![]() | (3) |
|
Two flicking strategies in palinurid lobsters
Flicking antennules collect both spatial and temporal information about a
plume's structure (reviewed in Crimaldi et
al., 2002; Weissburg,
2000
). Models by Crimaldi et al.
(2002
) show that flicking (1)
increases the number of concentration peaks (plume filaments) sampled per unit
time, (2) increases the probability of sampling a high concentration plume
filament and (3) permits two-dimensional sampling of the spatial structure of
the plume. The fast response and integration times of both Homarus
americanus (Nephropidae) and Panulirus argus (Palinuridae)
receptor cells suggest that information about odor concentration and filament
encounter can be acquired during and across flicks
(Fadool et al., 1993
; Gomez
and Atema,
1996a
,b
;
gomez et al.,
1994a
,b
,
1999
;
Moore and Atema, 1988
;
Schmiedel-Jakob et al.,
1989
).
P. argus, with its long antennules and slow flick rates, and P. elephas, with its short antennules and fast flick rates, use two different flicking strategies to sample the environment. Higher flick rates permit P. elephas to acquire shorter temporal samples of the environment than P. argus and, up to the temporal limits of the sensory receptors, can resolve shorter temporal fluctuations of filament concentrations as they move relative to the animal. Shorter antennules permit P. elephas to sample smaller areas of the plume than P. argus (Fig. 8) and can potentially resolve smaller spatial scale variations in plume filaments. P. argus samples a larger area of the plume per flick, which increases the probability of encountering an odor filament, but at the expense of small scale spatial resolution of the plume. By contrast, P. elephas samples small areas of water over shorter time scales and thus has higher spatial resolution of the plume compared with P. argus. However, if we take into account both (1) the probability of encountering an odor filament in the sampled area of a flick (high in P. argus and low in P. elephas) and (2) the probability of odor encounter based on the rate of flicking (low in P. argus and high in P. elephas), it remains to be determined whether these two species actually differ in the probability of encountering odor filaments.
Clearly, many factors influence evolutionary diversification of antennules
in spiny lobsters. Spiny lobsters inhabit a wide range of habitats, from
shallow reefs to deep-sea mud flats
(George and Main, 1967;
Holthuis, 1991
;
Kanciruk, 1980
;
Lozano-Alvarez and Biornes-Fourzan,
2001
; Sharp et al.,
1997
), and exhibit a range of social behaviors across species and
in the course of development (Childress
and Herrnkind, 1996
; Phillips
et al., 1980
). Odors play a central role in social behavior, and
detection is limited by concentration
(Childress and Herrnkind,
2001
; Ratchford and Eggleston,
1998
). While little is known of social and food searching behavior
in P. elephas (Hunter,
1999
), other spiny lobsters have been shown to rely on odor to
locate food (Zimmer-Faust and Case,
1983
; Zimmer-Faust et al.,
1985
), with Panulirus species foraging exceptionally long
distances compared with other palinurids
(Butler et al., 1999
;
MacDiarmid et al., 1991
). The
interplay between fluid dynamics, size, habitat and behavior is complex but
critical to informing our understanding of evolutionary changes in antennule
morphology. Perhaps the most fundamental conclusion to be drawn from the
present study is that, with their extraordinarily long flagella,
Panulirus is the unusual genus in palinurid lobsters. While P.
argus continues to be an informative model system, the next step is to
examine the evolutionary history and current function of these two palinurid
flicking strategies.
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Acknowledgments |
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Footnotes |
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References |
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Atema, J. (1995). Chemical signals in the marine environment: Dispersal, detection, and temporal signal analysis. Proc. Natl. Acad. Sci. USA 92, 62-66.[Abstract]
Atema, J. (1996). Eddy chemotaxis and odor
landscapes: exploration of nature with animal sensors. Biol.
Bull. 191,129
-138.
Atema, J. and Voigt, R. (1995). Behavior and sensory biology. In Biology of the Lobster Homarus americanus (ed. J. Factor), pp. 313-348. New York: Academic Press.
Baisre, J. A. (1994). Phyllosoma larvae and the phylogeny of the Palinuroidea (Crustacea: Decapoda): a review. Aust. J. Mar. Fresh. Res. 45,925 -944.
Butler, M. J., IV, MacDiarmid, A. B. and Booth, J. D. (1999). The cause and consequence of ontogenetic changes in social aggregation in New Zealand spiny lobsters. Mar. Ecol. Prog. Ser. 188,179 -191.
Cate, H. S. and Derby, C. D. (2001). Morphology and distribution of setae on the antennules of the Caribbean spiny lobster Panulirus argus reveal new types of bimodal chemo-mechanosensilla. Cell Tissue Res. 304,439 -454.[Medline]
Cate, H. S. and Derby, C. D. (2002). Hooded sensilla homologues: structural variations of a widely distributed bimodal chemomechanosensillum. J. Comp. Neurol. 444,435 -357.
Cheer, A. Y. L. and Koehl, M. A. R. (1987a). Fluid flow through filtering appendages of insects. IMA J. Math. App. Med. Biol. 4,185 -199.
Cheer, A. Y. L. and Koehl, M. A. R. (1987b). Paddles and rakes: fluid flow through bristled appendages of small organisms. J. Theor. Biol. 129,17 -39.
Childress, M. J. and Herrnkind, W. F. (1996). The ontogeny of social behaviour among juvenile Caribbean spiny lobsters. Anim. Behav. 51,675 -687.
Childress, M. J. and Herrnkind, W. F. (2001). The guide effect influence on the gregariousness of juvenile Caribbean spiny lobsters. Anim. Behav. 62,465 -472.
Crimaldi, J. P., Koehl, M. A. R. and Koseff, J. R. (2002). Effects of the resolution and kinematics of olfactory appendages on the interception of chemical signals in a turbulent odor plume. Environ. Fluid Mech. 2,35 -63.
Derby, C. 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. Fay, A. Popper and W. Tavolga). pp.365 -385. New York: Springer-Verlag.
Derby, C. D., Steullet, P., Horner, A. and Cate, H. (2001). The sensory basis of feeding behaviour in the Caribbean spiny lobster, Panulirus argus. Mar. Fresh. Res. 52,1339 -1350.
Døving, K. B., Dubois-Dauphin, M., Holley, A. and Jourdan, F. (1977). Functional anatomy of the olfactory organ of fish and the ciliary mechanism of water transport. Acta Zool. (Stock) 58,245 -255.
Dunham, D. W., Ciruna, K. A. and Harvey, H. H. (1997). Chemosensory role of antennules in the behavioral integration of feeding by the crayfish Cambarus bartonii. J. Crust. Biol. 171,27 -32.
Dykstra, M. J. (1992). Biological Electron Microscopy: Theory, Techniques, and Troubleshooting. New York: Plenum Press.
Fadool, D. A., Michel, W. C. and Ache, B. W.
(1993). Odor sensitivity of cultured lobster olfactory receptor
neurons is not dependent on process formation. J. Exp.
Biol. 174,215
-233.
George, R. W. and Main, A. R. (1967). The evolution of spiny lobsters (Palinuridae): a study of evolution in the marine environment. Evolution 21,803 -820.
Ghiradella, H. T., Case, J. F. and Cronshaw, J. (1968). Structure of aesthetascs in selected marine and terrestrial decapods: chemoreceptor morphology and environment. Am. Zool. 8,603 -621.[Medline]
Gleeson, R. A., Carr, W. E. S. and Trapido-Rosenthal, H. G. (1993). Morphological characteristics facilitate stimulus access and removal in the olfactory organ of the spiny lobster, Panulirus argus: insight from the design. Chem. Senses 18, 67-75.
Goldman, J. A. and Koehl, M. A. R. (2001).
Fluid dynamic design of lobster olfactory organs: high speed kinematic
analysis of antennule flicking by Panulirus argus. Chem.
Senses 26,385
-398.
Gomez, G. and Atema, J. (1996a). Temporal
resolution in olfaction II: time course of recovery from adaptation in lobster
chemoreceptor cells. J. Neurophysiol.
76,1340
-1343.
Gomez, G. and Atema, J. (1996b). Temporal
resolution in olfaction: stimulus integration time of lobster chemoreceptor
cells. J. Exp. Biol.
199,1771
-1779.
Gomez, G., Voigt, R. and Atema, J. (1994a). Frequency filter properties of lobster chemoreceptor cells determined with high-resolution stimulus measurement. J. Comp. Physiol. A 174,803 -811.
Gomez, G., Voigt, R. and Atema, J. (1994b). Tuning properties of chemoreceptor cells of the American lobster: temporal filters. In Olfaction and Taste, vol.XI (ed. K. Kurihara, N. Suzuki and H. Ogawa), pp.788 -789. Tokyo: Springer-Verlag.
Gomez, G., Voigt, R. and Atema, J. (1999). Temporal resolution in olfaction III: flicker fusion and concentration-dependent synchronization with stimulus pulse trains of antennular chemoreceptor cells in the American lobster. J. Comp. Physiol. A 185,427 -436.
Grünert, U. and Ache, B. (1988). Ultrastructure of the aesthetasc (olfactory) sensilla of the spiny lobster, Panulirus argus. Cell Tissue Res. 251,95 -103.
Halpern, M. and Kubie, J. L. (1980). Chemical access to the vomeronasal organs of garter snakes. Physiol. Behav. 24,367 -371.[Medline]
Hansen, B. and Tiselius, P. (1992). Flow through the feeding structures of suspension feeding zooplankton: a physical model approach. J. Plankton Res. 14,821 -834.
Holthuis, L. B. (1991). Marine lobsters of the world. In FAO Species Catalog, vol.13 , pp. 292. Rome: Food and Agriculture Organization of the United Nations.
Hunter, E. (1999). Biology of the European spiny lobster, Palinurus elephas (Fabricius, 1787) (Decapoda, Palinuridea). Crustaceana 72,545 -565.
Kanciruk, P. (1980). Ecology of juvenile and adult Palinuridae (spiny lobsters). In The Biology and Management of Lobsters, vol. 2 (ed. J. S. Cobb and B. F. Phillips), pp. 59-96. New York: Academic Press.
Koehl, M. A. R. (1993). Hairy little legs: feeding, smelling, and swimming at low Reynolds number. Contemp. Math. 141,33 -64.
Koehl, M. A. R. (1995). Fluid flow through hair-bearing appendages: feeding, smelling and swimming at low and intermediate Reynolds numbers. Soc. Exp. Biol. Symp. 49,157 -182.
Koehl, M. A. R. (1996). Small-scale fluid dynamics of olfactory antennae. Mar. Fresh. Behav. Physiol. 27,127 -141.
Koehl, M. A. R. (2000). Fluid dynamics of animal appendages that capture molecules: arthropod olfactory antennae. In Computational Modeling in Biological Fluid Dynamics, vol. 124 (ed. L. J. Fauci and S. Gueron), pp.97 -116. New York: Springer-Verlag.
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.
Kux, J., Zeiske, E. and Osawa, Y. (1988). Laser doppler velocimetry measurement in the model flow of a fish olfactory organ. Chem. Senses 13,257 -265.
Laverack, M. S. (1964). The antennular sense organs of Panulirus argus. Comp. Biochem. Physiol. 13,301 -321.[Medline]
Laverack, M. S. (1985). The diversity of chemoreceptors. In Sensory Biology of Aquatic Animals (ed. J. Atema, R. R. Fay, A. N. Popper and W. N. Tavolga), pp.287 -312. New York: Springer-Verlag.
Loudon, C., Best, B. A. and Koehl, M. A. R.
(1994). When does motion relative to neighboring surfaces alter
the flow through arrays of hairs? J. Exp. Biol.
193,233
-254.
Loudon, C. and Koehl, M. A. R. (2000). Sniffing
by a silkworm moth: wing fanning enhances air penetration through and
pheromone interception by antennae. J. Exp. Biol.
203,2977
-2990.
Lozano-Alvarez, E. and Biornes-Fourzan, P. (2001). Den choice and occupation patterns of shelters by two sympatric lobster species, Panulirus argus and Panulirus guttatus, under experimental conditions. Mar. Fresh. Res. 52,1145 -1155.
MacDiarmid, A. B., Hickey, B. and Maller, R. A. (1991). Daily movement patterns of the spiny lobsters Jasus edwarsii (Hutton) on a shallow reef in northern New Zealand. J. Exp. Mar. Biol. Ecol. 147,185 -205.
McWilliam, P. S. (1995). Evolution of the phyllosoma and puerulus phases of the spiny lobster genus Panulirus White. J. Crust. Biol. 15,542 -557.
Mead, K. S., Koehl, M. A. R. and O'Donnell, M. J. (1999). Stomatopod sniffing: the scaling of chemosensory sensillae and flicking behavior with body size. J. Exp. Mar. Biol. Ecol. 241,235 -261.
Moore, P. and Atema, J. (1988). A model of a temporal filter in chemoreception to extract directional information from a turbulent odor plume. Biol. Bull. 174,353 -363.
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., Atema, J. and Gerhardt, G. A. (1991a). Fluid dynamics and microscale chemical movement in the chemosensory appendages of the lobster, Homarus americanus. Chem. Senses 16,663 -674.
Moore, P. A. and Grills, J. L. (1999). Chemical orientation to food by the crayfish Orconectes rusticus: influence of hydrodynamics. Anim. Behav. 58,953 -963.[Medline]
Moore, P. A., Scholz, N. and Atema, J. (1991b). Chemical orientation of lobsters, Homarus americanus, in turbulent odor plumes. J. Chem. Ecol. 17,1293 -1307.
Oh, J. W. and Dunham, D. W. (1991). Chemical detection of conspecifics in the crayfish Procambarus clarkii: role of antennules. J. Chem. Ecol. 17,161 -166.
Patek, S. (2001). Signal producing morphology and the evolution of palinurid lobster communication. Dissertation in Biology, pp. 127. Durham: Duke University.
Phillips, B. F., Cobb, J. S. and George, R. W. (1980). General biology. In The Biology and Management of Lobsters: Physiology and Behavior, vol.1 (ed. J. S. Cobb and B. F. Phillips), pp.1 -82. New York: Academic Press.
Ptacek, M. B., Sarver, S. K., Childress, M. J. and Herrnkind, W. F. (2001). Molecular phylogeny of the spiny lobster genus Panulirus (Decapoda: Palinuridae). Mar. Fresh. Res. 52,1037 -1047.
Ratchford, S. G. and Eggleston, D. B. (1998). Size- and scale-dependent chemical attraction contribute to an ontogenetic shift in sociality. Anim. Behav. 56,1027 -1034.[Medline]
Reeder, P. B. and Ache, B. W. (1980). Chemotaxis in the Florida spiny lobster, Panulirus argus. Anim. Behav. 28,831 -839.
Schmiedel-Jakob, I., Anderson, P. A. V. and Ache, B. W.
(1989). Whole cell recording from lobster olfactory receptor
cells: responses to current and odor stimulation. J.
Neurophysiol. 61,994
-1000.
Schmitt, B. C. and Ache, B. W. (1979). Olfaction: responses of a decapod crustacean are enhanced by flicking. Science 205,204 -206.
Sharp, W. C., Hunt, J. H. and Lyons, W. G. (1997). Life history of the spotted spiny lobster, Panulirus guttatus, an obligate reef-dweller. Mar. Fresh. Res. 48,687 -698.
Snow, P. J. (1973). The antennular activities of the hermit crab, Pagurus alaskensis (Benedict). J. Exp. Biol. 58,745 -765.
Sokal, R. R. and Rohlf, F. J. (1981). Biometry. New York: Freeman.
Steullet, P., Dudar, O., Flavus, T., Zhou, M. and Derby, C.
D. (2001). Selective ablation of antennular sensilla on the
Caribbean spiny lobster Panulirus argus suggests that dual antennular
chemosensory pathways mediate odorant activation of searching and localization
of food. J. Exp. Biol.
204,4259
-4269.
Steullet, P., Krutzfeldt, D. R., Hamidani, G., Flavus, T., Ngo,
V. and Derby, C. D. (2002). Dual antennular chemosensory
pathways mediate odor-associative learning and odor discrimination in the
Caribbean spiny lobster Panulirus argus. J. Exp. Biol.
205,851
-867.
Sverdrup, H. U., Johnson, N. W. and Flemming, R. H. (1942). The Oceans: Their Physics, Chemistry, and General Biology. New York: Prentice-Hall Inc.
Trapido-Rosenthal, H. G., Carr, W. E. S. and Gleeson, R. A. (1987). Biochemistry of an olfactory purinergic system: dephosphorylation of excitatory nucleotides and uptake of adenosine. J. Neurochem. 49,1174 -1182.[Medline]
Vogel, S. (1994). Life in Moving Fluids. Princeton: Princeton University Press.
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 in finding prey.
J. Exp. Biol. 197,349
-375.
Winter, D. A. (1990). Biomechanics and Motor Control of Human Movement. New York: John Wiley & Sons, Inc.
Zar, J. H. (1999). Biostatistical Analysis. New Jersey: Prentice-Hall.
Zimmer-Faust, R. K. and Case, J. F. (1983). A proposed dual role of odor in foraging by the California spiny lobster, Panulirus interruptus (Randall). Biol. Bull. 164,341 -353.
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.
Zimmer-Faust, R. K., Tyre, J. E. and Case, J. F. (1985). Chemical attraction causing aggregation in the spiny lobster, Panulirus interruptus and its probable ecological significance. Biol. Bull. 169,106 -118.