Mar. Freshwater Res.
© CSIRO 2001 10.1071/MF01099 1323-1650/01/081339
The sensory basis of feeding behaviour in the Caribbean spiny lobster,
Charles D. Derby, Pascal Steullet, Amy J. Horner, and Holly S. Cate
Department of Biology and Center for Behavioral Neuroscience, Georgia State University, Atlanta, Georgia
30302-4010, USA. email: email@example.com
paper discusses the ways in which the sensory systems of the Caribbean spiny lobster,
particularly its chemosensory systems, are involved in feeding behaviour. It addresses the neural mechanisms of
three aspects of their food-finding ability: detection, identification, and discrimination of natural food odours; the
effect of learning on responses to food odours; the mechanisms by which spiny lobsters orient to odours from a
distance under natural flow conditions. It demonstrates that the olfactory organ of spiny lobsters might use across-
neuron response patterns in discriminating odour quality; that the hedonic value of food can be modified by
experience, including associative and nonassociative conditioning; that spiny lobsters can readily orient to distant
odour sources; and that both chemo- and mechanosensory antennular input are important in this behaviour. Either
aesthetasc or nonaesthetasc chemosensory pathways can be used in identifying odour quality, mediating learned
behaviours, and permitting orientation to the source of distant odours. Studying the neuroethology of feeding
behaviour helps us understand how spiny lobsters are adapted to living in complex and variable environments.
A complex nervous system enables spiny lobsters to have a rich behavioural repertoire. The present
Crustacea, olfaction, chemical sense, chemoreception, mechanoreception, orientation,
The nervous system of spiny lobsters contains an enormous
number and diversity of neurons. For example, receptor
neurons number well over 1 million (Grünert and Ache
1988; Laverack 1988
; Cate and Derby, 2000, 2001), and
the brain has many sensory and integrative centres, each
with a different, complex organization (Maynard 1966;
Sandeman 1990; Sandeman
1993; Schmidt and Ache 1996
perform a rich array of behaviours, show extensive
behavioural plasticity, and have impressive learning
abilities (Winn and Olla 1972; Krasne 1973; Abramson and
Feinman 1990; Feinman
Derby 2000). Studying their nervous system and
behavioural abilities, and the causal links between the two,
gives us a better understanding of how spiny lobsters and
other crustaceans have adapted to living in complex and
The chemosensory pathways are a prominent part of the
nervous system of spiny lobsters and other crustaceans. The
first antennae (antennules) alone have over 500,000
chemosensory neurons (Grünert and Ache 1988; Steullet
; Cate and Derby 2001), and six paired neuropils
. 1992; Mellon and Alones
). These animals also
. 1990; Pereyra
(olfactory lobes, lateral antennular neuropils, median
antennular neuropils, accessory lobes, terminal medullae,
and hemiellipsoid bodies) are directly or indirectly
connected to this antennular input (Sandeman
Schmidt and Ache 1996
It is therefore not surprising that spiny lobsters use their
chemical senses in many behaviours, including feeding
(Reeder and Ache 1980; Zimmer-Faust
shelter selection (Ratchford and Eggleston 1998, 2000;
Zimmer-Faust 1987). Whether they also use their chemical
senses in larval settlement, avoiding predators, mate
selection, social interactions among conspecifics, or other
intra- and interspecific interactions remains to be
determined, although these functions have been
demonstrated in other crustaceans (Caldwell and Dingle
1985; Carr 1988; Gleeson 1991; Hazlett 1994
Schoolmaster 1998; Karavanich and Atema 1998
Zulandt Schneider and Moore 1999, 2000). Feeding
behaviour is the best studied of the chemosensory
behaviours in spiny lobsters, especially in terms of sensory
mechanisms. The present paper summarizes our current
understanding of this topic.
. 1996) and
; Hazlett and
1340Charles D. Derby
To use its chemical senses to find food, an animal must
successfully perform several tasks involving sensory,
integrative, and motor functions. First, it must identify the
nature of the chemical signals. It must detect and distinguish
relevant chemical signals against background chemicals,
and it must determine the qualities (
structures), quantities (
., concentrations), and locations
., spatiotemporal dynamics) of these signals. Second, it
must decide whether or not to search for the sources of those
signals. To do so, it must compare this chemosensory input
with innate or learned neural templates and make
behavioural choices whether or not to respond, and if so,
how to respond. Third, it must locate the source of the
signals by orienting to them from a distance using available
cues, such as the spatiotemporal distribution of chemical
and hydrodynamic cues.
Here, we review work that shows that spiny lobsters can
accomplish all of these tasks. We focus on the Caribbean
of choice in neurobiological studies of the chemical senses.
First, we describe mechanisms of detection, identification,
and discrimination of behaviourally relevant chemical
signals, especially complex food-related mixtures. Second,
we show that spiny lobsters can change their responses to
chemical signals in adaptive ways, as a result of experiences
such as associative learning. Third, we explain sensory
mechanisms involved in orientation toward distant chemical
signals under natural flow conditions.
, which has been an organism
Detection and discrimination of chemical signals
The first tasks that spiny lobsters must accomplish during
feeding—detecting, identifying, and discriminating the
nature of chemical cues—are accomplished through their
impressive chemosensory systems. Chemical sensors are
present on most body surfaces, especially the first antennae
(= antennules), second antennae, legs, and mouthparts, but
also the cephalothorax, abdomen, and telson (Fig. 1
(Laverack 1964, 1988
; Grünert and Ache 1988; Derby
. 1993; Cate and Derby 2000, 2001). The
chemosensors are organized as sensilla, which are cuticular
extensions of the body surface that are innervated by the
dendrites of chemosensory neurons. The aesthetascs are a
prominent type of chemosensor that are located only on the
distal half of the antennular lateral flagella; they are the only
known unimodal chemosensors (Laverack 1964; Grünert
and Ache 1988; Derby 1989; Cate and Derby 2001) (Figs
). All of the other known chemosensilla on
are bimodal, being innervated by both
chemosensory neurons and mechanosensory neurons (Cate
and Derby 2000, 2001). These include hooded sensilla (Figs
) and simple sensilla (Figs 1
hooded sensilla are a particularly interesting sensillar type,
because they are abundantly located over most of the
animal’s body, including the lateral and medial antennular
flagella, antennae, legs, mouthparts, cephalothorax,
abdomen, and telson (Cate and Derby 2000, 2001).
Different chemosensors act sequentially during the
feeding behaviour of lobsters: antennular chemoreceptors
initiate searching and orientation toward the source of a
distant chemical stimulus (Reeder and Ache 1980; Devine
and Atema 1982; Steullet
control local grasping reflexes; and mouthpart
chemoreceptors mediate the decision to ingest food (Derby
and Atema 1982). The roles of the chemoreceptors on the
cephalothorax and abdomen have not been examined.
The neural basis for discrimination of food odours has
been extensively studied in the chemosensory neurons of the
antennules. The first step in this process—the transduction
of chemical information into electrical signals by antennular
receptor neurons—is known in cellular and molecular detail
that reveals the function of receptor proteins, G-proteins,
second-messenger cascades, ion channels, transporters, and
enzymes in detecting odorant molecules (Carr
Ache and Zhainazarov 1995; Olson and Derby 1995;
. 1997; Xu
Ache 1999; Munger
. 2000). Beyond chemosensory
transduction, how chemical quality and quantity are
encoded by the chemosensory neurons of the antennules has
also been well studied in lobsters, both the spiny lobster
and the American lobster
(for reviews, see Atema
Derby and Atema 1988; Derby 2000). Each antennule has
hundreds of thousands of chemoreceptor neurons (Grünert
and Ache 1988; Cate and Derby 2000, 2001). The antennule
as a whole is sensitive to many different odorants,
particularly to small, water-soluble molecules such as amino
acids, amines, nucleotides, and sometimes sugars and
peptides (Carr 1988). Yet each antennular chemoreceptor
neuron responds to a limited subset of these chemical
stimulants. Individual neurons are not specifically tuned to
respond to only one complex stimulus; most cells respond to
different degrees to all tested complex food mixtures
(Girardot and Derby 1990
individual neurons to the components of these mixtures is
often complex: typically, each neuron is excited by some
odour compounds, is inhibited by others, and gives
complex, nonlinear, often unpredictable responses to
combinations of odour compounds (Ache 1989; Atema
. 1989; Cromarty and Derby 1998; Derby
and Atema 1988; Derby 2000). Thus, chemoreceptor
neurons of spiny lobsters are complex peripheral processing
How then is chemical quality determined? The likely
answer is ‘across-neuron response patterns’, also called
‘distributed’ or ‘ensemble’ neural response patterns. An
across-neuron pattern distinguishes one odorant from
another by differences in the relative activity among most or
all members of a neuronal population, rather than by the
); leg chemoreceptors
. 1998; Zhainazarov and
. 1989; Derby
). The responsiveness of
Sensory basis of feeding behaviour,
presence or absence of activity in a specific subset of
specialized neurons. Support for the idea that the antennular
chemosensory system of
response patterns in quality coding comes from studies of
responses of receptor neurons to different sets of food-
related chemicals, including simple stimuli (single
compounds), complex artificial stimuli (binary and
multicomponent mixtures), and complex natural stimuli
(tissue extracts from potential prey species). Figure 2 shows
across-neuron response patterns for four different
multicomponent artificial stimuli representing food—crab
mixture, shrimp mixture, mullet mixture, and oyster
mixture. The across-neuron response patterns for these
mixtures are different from each other (Fig. 2
), and these
differences are highly correlated with differences in both the
animal’s perceived quality of the mixtures (Fig. 2
mixtures’ compositions (Fig. 2
mixture, which have the most similar compositions among
these four mixtures, generate the most similar across-neuron
response patterns and are perceived by lobsters as being
most similar. Crab mixture and oyster mixture, on the other
hand, have highly dissimilar compositions, evoke highly
different across-neuron response patterns, and are perceived
by lobsters as being more dissimilar in quality. Spiny
lobsters therefore appear to use sensory information in the
form of across-neuron response patterns in their antennular
chemosensory system to discriminate the quality of natural,
complex chemical stimuli.
) and the
). Crab mixture and shrimp
appendages, including both flagella of the first antennae (antennules), second antennae, mouthparts, legs, cephalothorax, abdomen, and
telson. Modified from Grünert and Ache (1988). (
) Scanning electron micrograph of the distal region of the lateral flagellum of the
antennule, showing some of the setae unique to this region: aesthetasc sensilla (a), guard setae (gs), companion setae (cs), and asymmetric
setae (as). (
) Hooded sensilla, which are bimodal (chemo-mechano) sensors found on most body surfaces; examples shown here are
from the cephalothorax (
) and the antennular lateral flagellum (
found on most body surfaces; examples shown here are a medium simple sensillum (
Sensors on the Caribbean spiny lobster,
) Chemo- and mechanosensors are ubiquitous on the body and
) Simple sensilla, which are bimodal (chemo-mechano) sensors
) and a long simple sensillum (
) on the antennule.
1342Charles D. Derby
(A) Neural Distributed Codes
(B) Behavioral Discrimination
Fig. 2. Spiny lobsters might use across-neuron response patterns to assess differences in stimulus quality of four complex food-related chemical
mixtures. Stimuli are crab, shrimp, oyster, and mullet mixtures, which are 41-component artificial mixtures containing amino acids, amines,
nucleotides, nucleosides, quaternary ammonium compounds, and organic acids at the concentrations that each occurs in the tissue from
representative species (Carr 1988). (A) Relative similarities between mixtures according to across-neuron response patterns for a population of 30
receptor neurons in the lateral antennular flagellum. Electrophysiological responses were recorded for each of the 30 neurons to the four mixtures,
each at three concentrations (C1, S1, M1, and O1 are crab, shrimp, and oyster mixtures at 5 µM, respectively; C2, S2, M2, and O2 are these mixtures
at 50 µM; and C3, S3, M3, and O3 are at 500 µM); responses were quantified as number of action potentials during 5 s of stimulation. The similarity
between the across-neuron pattern responses of these 30 cells to each pair of mixtures was quantified by means of squared Euclidean distances; this
pairwise analysis for all pairs of stimuli resulted in a 12 × 12 matrix of similarity measures. This matrix was then applied to multidimensional
scaling, which is a type of multivariate analysis, with the goal of reducing this matrix to as few ‘dimensions’ as possible while still explaining >90%
of the variance in the matrix. In this case, the three-dimensional solution shown in this figure did so. Each of the three dimensions explains some,
though differing amounts, of the variability in the across-neuron pattern responses due to stimulus type and/or concentration; thus, in this graph, as
in all multidimensional scaling, the dimensions do not have ‘labels’. In this figure, each point represents the across-neuron response pattern for one
stimulus (e.g., C3 is crab mixture at 500 µM), and each shaded triangle represents the stimulus space for a two-log-unit concentration range of each
mixture (for C, this is the stimulus space represented by 5–500 µM crab mixture). In this figure, the distance between stimuli or stimulus space is
correlated with the similarity in across-neuron response patterns; thus, stimuli close to each other have relatively similar across-neuron response
patterns, and stimuli distant from each other have relatively dissimilar across-neuron response patterns. Thus, this figure shows that the stimulus
space (and therefore across-neuron pattern responses) for crab mixture is relatively similar to that for shrimp mixture but relatively dissimilar to that
for oyster mixture. From Girardot and Derby (1988). (B) Relative similarities between mixtures according to behavioural studies of discrimination.
The data set used in this analysis was behavioural responses of lobsters to crab mixture (CM), shrimp mixture (SM), mullet mixture (MM), and
oyster mixture (OM), each at two concentrations (50 and 500 µM). The data were collected from four groups of three animals; members of each
group were aversively conditioned to both concentrations of a single mixture before generalization testing for the other three mixtures. Behavioural
responses were ‘aversion values’, based on changes in appetitive and aversion responses due to aversive conditioning. Aversive conditioning
followed by generalization testing is a standard procedure for determining discrimination abilities of animals. In this analysis, similarities in the
aversion values were determined for each pair of stimuli by means of Euclidean distances, and these similarities were used to construct an 8 × 8
matrix. As in Fig. 2A, this matrix of similarities was used in multidimensional scaling to simplify the data set to the minimum number of
‘dimensions’ sufficient to describe >90% of the data set’s variability. In this case, a two-dimensional solution sufficed. The dimensions of this
figure do not have labels, as explained above under Fig. 2A. In this two-dimensional solution, distances between the stimuli are correlated with
perceptual similarity; stimuli close to each other are perceived by lobsters as being more similar than are stimuli farther from each other. Thus,
lobsters perceive the two concentrations of crab mixture as relatively similar to each other, and relatively similar to the two concentrations of shrimp
mixture, but relatively different from oyster mixture or mullet mixture. From Fine-Levy et al. (1989). (C) Relative similarities in the chemical
compositions of the mixtures. A cluster analysis, which is another type of multivariate analysis, was used to evaluate similarities in the chemical
compositions of the four mixtures. The similarity in the chemical composition of each pair of mixtures was evaluated from Pearson product-
moment correlation coefficients as distance measures based on the concentrations of the 41 chemical components of the mixtures. A 4 × 4 matrix
of these similarity values was created and used in the cluster analysis, the results of which are depicted as a dendrogram. Mixtures joined at a short
cluster distance have more similar compositions than do mixtures joined at longer distances. Thus, crab and shrimp mixtures have compositions
relatively similar to each other but different from oyster or mullet mixtures. Only four points appear in this figure, compared to the 12 points in Figs
2A and 2B, because the multivariate analysis using Pearson correlation coefficients shows that three concentrations for each mixture type are
identical. From Fine-Levy et al. (1988).
Sensory basis of feeding behaviour,
Chemical concentration can be encoded by the overall
intensity of responses of the antennular chemoreceptor cells
(reviewed by Derby and Atema 1988; Ache 1989; Derby et
al. 1989; Derby 2000). An independence of codes for
chemical type and quantity would allow constancy in the
perceived quality of an odour in spite of the large
fluctuations in concentrations that occur in nature. Support
for this independence in P. argus comes from three
observations. First, the mean response from a population of
antennular chemoreceptor neurons is highly correlated with
stimulus concentration (Girardot and Derby 1988, 1990a;
Daniel et al. 1996). Second, changes in stimulus
concentration by as much as two orders of magnitude have a
relatively small effect on the across-neuron response
patterns for stimulus quality (Fig. 2A) (Girardot and Derby
1990a). Third, behavioural discriminations of chemical
quality are relatively insensitive to changes in chemical
intensity (Fig. 2B) (Fine-Levy et al. 1989; Fine-Levy and
Derby 1991). An alternative theory of coding of stimulus
quality has been proposed for H. americanus: that both
chemical concentration and quality are encoded by across-
neuron response patterns (Johnson et al. 1992; Merrill et al.
Whereas across-neuron response patterns are probably
used by spiny lobsters in encoding the quality of food-
associated chemicals, other chemical signals, such as
pheromones, might be encoded differently. In many
animals, pheromones are encoded by specialized receptor
neurons, which function as ‘labelled lines’ rather than in
across-neuron response patterns (Ache 1991, Hildebrand
% Difference in Search Response between
Conditioned and Unconditioned Lobsters
% Difference in Search Response between
Conditioned and Unconditioned Lobsters
Blends of AMP:taurine (x 10-2 mM)
A. Generalization Conditioning to Complex Mixture
B. Discrimination Conditioning to Binary Mixture
Fig. 3. Summary of results of behavioural discrimination experiments showing that both aesthetasc sensilla and nonaesthetasc sensilla are
sufficient but not necessary for odour learning and discrimination. Discrimination was examined in intact animals, aesthetasc-ablated animals,
and nonaesthetasc-ablated animals. Each of these treatments involved two groups of animals: one group conditioned to avoid one mixture (crab
mixture in (A) and 99.9:0.1 blend ratio of AMP:taurine in (B)) and another group that was unconditioned. The experiments shown here used a
total of 10 groups, each consisting of 10–20 animals. In (A), animals were subjected to generalization conditioning; that is, during the
conditioning phase, only one mixture, crab mixture, was presented, and it was always paired with the aversive stimulus. In (B), animals were
subjected to discrimination conditioning; that is, during the conditioning phase, one blend ratio (99.9:0.1) was paired with the aversive stimulus,
and the other three blend ratios were also presented but explicitly unpaired with the aversive stimulus. In postconditioning testing, responses
(quantified as duration of searching behaviour) were measured for all mixtures (crab, shrimp, mullet, and inverse crab mixtures were tested in
(A), and AMP:taurine blend ratios of 99.9:0.1, 99:1, 90:10, and 50:50 were tested in (B)). Crab, shrimp, and mullet mixtures are the 41-
component mixtures of Fig. 2. Inverse crab mixture contains the same 41 components as crab mixture, with the following difference: the
component in inverse crab with the highest concentration is the component in crab with the lowest concentration; the component in inverse crab
with the second highest concentration is the component in crab with the second lowest concentration; and so forth, until the component in
inverse crab with the lowest concentration is the component in crab with the highest concentration. The ability of animals to learn the
conditioned task is quantified in the ordinate, which shows the relative difference between responses of conditioned and unconditioned animals
to the mixtures. This measure can reveal three events: (1) aversive learning of the conditioned stimulus is indicated by a negative ordinal value
(i.e., aversive conditioning resulted in a decrease in lobsters’ appetitive searching for the food odour); (2) generalization between the
conditioned and unconditioned stimuli (i.e., perception by lobsters of some similarity between the two stimuli) is indicated by a negative value
for the unconditioned stimulus; and (3) ability to discriminate between conditioned and unconditioned stimuli is indicated by a significant
difference between their ordinal values. Thus, learning of the conditioned mixture is demonstrated for all three groups of animals in (A) and
both groups in (B) by the negative values for the conditioned mixture (crab in (A) and 99.9:0.1 AMP:taurine in (B)). Second, animals can
discriminate between the conditioned and unconditioned mixtures in both (A) and (B), as demonstrated by the difference in values between the
conditioned mixtures and the unconditioned ones. Third, in (A) intact animals were better at discriminating between the conditioned and
unconditioned mixtures than were either aesthetasc-ablated or nonaesthetasc-ablated animals, which performed similarly. In (B), however,
intact and aesthetasc-ablated lobsters performed similarly, thus showing that lobsters without aesthetascs are able to perform difficult
discriminations (i.e., between different blend ratios of the same binary mixture).
1344 Charles D. Derby et al.
and Shepherd 1997). Neural processing of pheromones has
scarcely been studied in crustaceans, particularly the
decapods, because the molecular identity of their
pheromones is largely unknown (Gleeson 1991).
Antennular chemoreceptors provide the input that leads
to initial discrimination of stimuli and the decision whether
or not to initiate a search (Reeder and Ache 1980; Devine
and Atema 1982), but the antennules bear many setal types
(Fig. 1), including setae that are known to be innervated and
are therefore called ‘sensilla’. Antennular chemosensilla
include aesthetascs, hooded sensilla, and several types of
simple sensilla (Laverack 1964; Grünert and Ache 1988;
Cate and Derby 2000, 2001). Other setae, whose innervation
has not been studied, include guard setae, companion setae,
asymmetric setae, and plumose setae. Here we collectively
call all antennular setae other than aesthetascs
The identity of the setal types responsible for antennule-
mediated odour discrimination is not obvious and
determining it requires experimental manipulation. We
examined this issue by studying the behaviour of spiny
lobsters in which specific antennular setal types (such as
aesthetasc sensilla, nonaesthetasc setae, all antennular setae)
had been deafferented and comparing the behaviours of
these ablated animals with those of control animals that had
received no surgical treatment. We examined behavioural
discrimination by aversively conditioning lobsters to avoid
previously stimulatory chemicals and subsequently testing
their generalization to other chemical stimuli (Steullet et al.
1999, 2000b). Intensity of response to odours was quantified
as the duration of searching behaviour. Results showed that
antennular chemoreceptors are important for evoking these
searching behaviours, because animals without them
responded significantly less than intact animals. Animals
from which either the aesthetasc or nonaesthetasc setae had
been removed still responded to the mixtures, learned the
conditioning task, and discriminated between the
conditioned and nonconditioned mixtures (Fig. 3), so
aesthetasc chemoreceptors are sufficient but not necessary
for lobsters to discriminate between highly related chemical
mixtures. Likewise nonaesthetasc antennular
chemoreceptors are sufficient but not necessary. We have
observed the same results under a variety of experimental
conditions. These include using two stimulus sets—a set of
multicomponent artificial food mixtures (Fig. 3A) and a set
of binary mixtures containing the same components
(adenosine-5’-monophosphate and taurine) but at different
blend ratios (from 99.9:0.1 to 50:50) (Fig. 3B)—and using
two training and discrimination tasks—generalization
conditioning (Fig. 3A) and discrimination conditioning (Fig.
3B). Together, these experiments show that there is overlap
in the function of the aesthetasc and nonaesthetasc receptor
neurons in chemical discrimination, and this overlap
functions in different biological contexts. There may be
differences in the discriminations mediated by the
aesthetasc and nonaesthetasc systems of spiny lobsters, such
as in their responsiveness to social or sex pheromones, but
these differences have not yet been identified.
Learning about chemical signals
After identifying a chemical signal, a lobster must decide
whether to search for its source. In this respect, lobsters
show impressive behavioural plasticity; experience and
learning are important. This plasticity is expected from and
beneficial to animals such as lobsters that can live for many
years, are omnivorous, live in many different environments,
and consequently are exposed to different chemical stimuli
that can assume of variety of meanings.
An example of plasticity in chemical responsiveness is
that the hedonic value of food can be modified by
experience. Spiny lobsters can learn through negative
conditioning to avoid naturally attractive chemicals, and
they can learn through positive conditioning to increase
their attraction to other food-related chemicals. For
example, as described in the previous section on
chemosensory discrimination, spiny lobsters can be
associatively conditioned to stop responding to food odours
that are normally excitatory and attractive if those stimuli
are paired with aversive stimuli (Fine-Levy et al. 1988,
1989; Lynn et al. 1994; Livermore et al. 1997). We used as
the aversive unconditioned stimulus a ‘pseudopredator’ (a
black object moved rapidly toward the animal) to simulate
natural conditions, such as a situation where lobsters are
attracted to food odours but while searching are chased by a
predator. The rapid learning of this conditioning task (5–10
trials) and its several-day duration, together with our failures
to condition animals with unnatural aversive stimuli such as
electric shock (Fine-Levy et al. 1988), show that this is a
powerful and biologically relevant form of learning. Spiny
lobsters can also learn by habituation to stop responding to
previously attractive food chemicals (Daniel and Derby
1988). Such nonassociative learning requires many trials,
however, presumably because food chemicals are normally
highly attractive and have positive hedonic values, and it is
therefore not adaptive for animals to habituate quickly to
innately positive stimuli that have not received concomitant
Spiny lobsters can learn different features of food-related
complex chemical cues, depending on the context of
learning and the available cues. A mixture might be
perceived either as a combination of its individual
components (i.e., elemental cues) or as a mixture-unique
stimulus (i.e., configural cue). Which of these cues
dominates perception is influenced by the salience of each,
including past experience with mixtures and their
components. Spiny lobsters are able to learn to respond to
either elemental or configural cues (Livermore et al. 1997),
as can other animals from honey bees to rats (Rescorla et al.
Sensory basis of feeding behaviour, P. argus
1985; Rudy and Sutherland 1992; Smith 1996). This ability
highlights the sophistication of chemosensory processing
and learning by lobsters.
Other interesting forms of learning have been
demonstrated in some crustacean species but not in spiny
lobsters. These include one-trial food-aversion learning
(Wight et al. 1990), learned preferences for the odour of
experienced foods (Derby and Atema 1981; Hazlett 1994b),
learning of the identity of individual conspecifics or
dominance status during social encounters (Caldwell and
Dingle 1985; Hazlett 1994a; Hazlett and Schoolmaster
1998; Karavanich and Atema 1998a, 1998b, Zulandt
Schneider and Moore 1999, 2000), and other learned
behaviours (Winn and Olla 1972; Krasne 1973; Abramson
and Feinman 1990; Feinman et al. 1990; Pereyra et al.
Orientation to distant chemical signals
After sensing a food odour and deciding to search for it,
spiny lobsters must locate that food using available cues.
Their ability to do so has been studied in a laboratory flume
that produces controlled flow conditions mimicking those
found in nature (Fig. 4A) (Horner et al. 2000). This study
shows that spiny lobsters can efficiently and reliably orient
to odour sources 2 m away (Figs 4B and 5). Similar abilities
have also been demonstrated in other crustaceans, including
American lobsters (Moore et al. 1991; Grasso et al. 1998a),
blue crabs (Weissburg and Zimmer-Faust 1993, 1994;
A. Orientation paths of intact lobsters (n = 14)
B. Orientation paths of lobsters with aesthetascs
ablated (n = 10)
D. Orientation paths of lobsters with non-
aesthetasc chemoreceptors ablated (n = 4)
C. Orientation paths of lobsters with non-aesthetasc
chemo- and mechanoreceptors ablated (n = 5)
Fig. 4. Paths of spiny lobsters in odour plumes produced in a laboratory flume. (A) A 2-m region of an 8000-L flume located at Georgia
Institute of Technology. The chemical stimulus was 3 gm/L shrimp extract released by a peristaltic pump at 5 cm/s, which is the same velocity
at which sea water runs through the flume. The dimensions of the flume and lobster are shown to scale in all parts of this figure. A trial
consisted of placing an animal in the cage, releasing an odour from the source, and videotaping the behavioural response for 10 min with a
CCD camera above the flume. (B–E) Orientation paths of individual animals from four treatment groups. The videotaped movements of each
lobster that successfully found the odour source were later digitized and plotted with Motion Analysis® software. The number of individual
orientation tracks, each from a different lobster, is shown on each figure for each treatment group. (B) Intact animals: Animals with no
ablations. (C) Animals with aesthetascs ablated: only aesthetascs and asymmetric setae were surgically ablated; all other antennular setae
(nonaesthetasc chemo/mechanoreceptors) were intact. (D) Animals with nonaesthetasc chemo- and mechanoreceptors ablated: all antennular
nonaesthetasc setae were surgically ablated and/or covered with cyanoacrylate glue; aesthetasc chemoreceptors were intact. (E) Animals with
nonaesthetasc chemoreceptors ablated: all antennular nonaesthetasc chemoreceptors were ablated through shaving and gluing of
nonaesthetasc sensilla in the distal region of the lateral flagella and through distilled-water ablation of those on the remainder of the flagella.
The distilled-water ablation technique consists of exposing the area of interest to distilled water for 5 min, as described by Derby and Atema
(1982). This technique inactivates all chemoreceptors while sparing at least some mechanoreceptor activity. These animals thus lack functional
nonaesthetasc chemoreceptors but have functional nonaesthetasc mechanoreceptors as well as aesthetasc chemoreceptors.
1346Charles D. Derby et al.
Zimmer-Faust et al. 1995), and crayfish (Moore and Grills
1999; T. Breithaupt, pers. comm.).
What receptors are used in chemo-orientation of
lobsters? The importance of antennules in odour orientation
has been previously demonstrated in both P. argus (Reeder
and Ache 1980) and H. americanus (Devine and Atema
1982; Grasso et al. 1998a), but the antennules have many
different setal types, including unimodal chemosensilla
(aesthetascs), bimodal chemomechanosensilla (hooded
sensilla and simple sensilla), and many others (Fig. 1).
Which of these setae are responsible for chemical
orientation is not known, although the prominent
aesthetascs are often assumed to be the mediators. We
studied orientation of animals from which various types of
setae had been eliminated (Horner et al. 2000) (Figs 4 and
5). Intact animals readily initiated searching (i.e., left the
cage shelter), usually found the odour source, and did so
rapidly via a direct path (Figs 4B and 5). Animals without
any functional antennular chemoreceptors but with intact
antennular mechanoreceptors (i.e., ‘aesthetasc and
nonaesthetasc chemoreceptors ablated’ in Fig. 5A) only
occasionally initiated a search and located the source in only
1 of 17 trials (Fig. 5), supporting the importance of
antennular chemoreceptors to this behaviour. Animals in all
other treatment groups found the odour source with
approximately the same probability. Animals with
aesthetascs ablated (Figs 4C and 5) and animals with
antennular nonaesthetasc chemoreceptors ablated (Figs 4D
and 5) showed similar behaviour. Both groups were as likely
as intact animals to locate the odour source (Fig. 5A), but
search efficiency was slightly poorer in these two groups
than in intact animals—their paths to the odour source were
more circuitous, and the total search time was longer.
Interestingly, animals lacking only antennular nonaesthetasc
n = 10n = 4n = 14n = 4
n = 21n = 8 n = 14n = 6n = 17
Percentage of Animals
Locating the Odor Source
A.Net-to-Gross Displacement RatioB.
Time to Locate the Odor Source
n = 15n = 6n = 10n = 4
Non-aesthetasc Chemo- and
Aesthetasc and Non-aesthetasc
Fig. 5. Effects of ablations of antennular setae on orientation of spiny lobsters to odours. These figures are based on the data from the
orientation tracks in Fig. 4. Sample size for each treatment group is shown in the corresponding panel. Treatments are as in Fig. 4, except also
shown in (A) are results for animals with ‘aesthetasc and nonaesthetasc chemoreceptors ablated’. This group had both the lateral and medial
flagella ablated by the distilled-water technique described in the legend of Fig. 4 for animals with ‘nonaesthetasc chemoreceptors ablated’.
Because only 1 of 17 animals in this group located the odour sources, this group was not included in Figs 5B and 5C. (A) Percentage of animals
locating the odour source. This panel shows the likelihood that tested animals will successfully orient to the odour source within a 10-min trial.
(B) Net-to-gross displacement ratio. This ratio is calculated from the orientation paths, as the ratio of the Euclidean distance from cage to odour
source to the total distance travelled by the animal. A value of one is a direct track to the source, and values approaching zero represent
increasingly more indirect paths. Values are means ± standard error of the mean. (C) Time to locate the odour source. Values are means ±
standard error of the mean.
Sensory basis of feeding behaviour, P. argus
chemoreceptors (‘nonaesthetasc chemoreceptors ablated’:
Figs 4E and 5) were better at orienting than were animals
lacking both nonaesthetasc chemo- and mechanoreceptors
(Figs 4D and 5). This result points to the importance of
antennular mechanoreceptors to orientation to odours in
Taken together, our results on P. argus suggest that
antennules are necessary for initiating and probably for
maintaining searching for distant odours and that both
antennular chemoreceptors and mechanoreceptors
contribute. The setae that mediate this behaviour are
distributed and diverse, because chemoreceptors in either
aesthetasc or nonaesthetasc setae are sufficient but not
necessary for successful orientation behaviour. Antennular
mechanoreceptors contribute to orientation to odours,
presumably by providing information about flow cues. The
physiology of the antennular neurons involved in orientation
to distant chemical signals under natural flow conditions is
beginning to be understood, including their ability to resolve
the spatiotemporal distribution of chemical and mechanical
flow cues. Lobster antennular receptor neurons can follow
chemical stimulus pulses at frequencies as high as four
pulses per second (Marschall and Ache 1989; Gomez et al.
1999). These cellular properties allow resolution of the
spatiotemporal patterns of chemical signals produced in
their natural environment (Moore and Atema 1988; Atema
1995; Weissburg 2000; Zimmer and Butman 2000). Even
better studied are assorted sensillar mechanoreceptor
neurons, which have response properties that allow them to
follow dynamic changes in water flow under natural
conditions, including detecting the presence and
characteristics of eddies (Tautz and Sandeman 1980;
Sandeman 1989; Breithaupt and Tautz 1990; Bleckmann et
al. 1991; Weissburg 1997).
Exactly how chemo- and mechanoreceptors are used in
combination in mediating orientation is not known,
although several hypotheses based on work on other
crustaceans have been suggested. One proposed mechanism,
based on experimental work on the clawed lobster Homarus
americanus, is that animals might orient in and find an
odour source using only spatiotemporal features of chemical
cues (Moore and Atema 1988; Moore et al. 1991; Atema
1996). This theory has been tested with modelling, robots,
and animals (Grasso et al. 1998a, 1998b, 1999), and the
results have generally not supported it but have lead to a
second proposed mechanism—that the spatiotemporal
distribution of not only chemical cues but also
hydrodynamic cues is used in orientation (Atema 1996;
Grasso et al. 1998a, 1999; Moore and Grills 1999). The
mechanism might be as relatively simple as an odour-
activated rheotaxis, in which odour stimulation initiates
search while the direction of current flow provides
orientation cues (Weissburg and Zimmer-Faust 1993, 1994;
Zimmer-Faust et al. 1995; T. Breithaupt, pers. comm.). The
mechanism could, however, be more complex. For example,
substantial chemical and mechanical information might be
present in the odour-scented eddies themselves that would
indicate the location of the source (Atema 1996; Grasso et
al. 1998a, 1999; Moore and Grills 1999). More
experimentation is necessary to ascertain whether these or
other mechanisms can explain orientation in crustaceans,
including P. argus.
We thank V. Ngo, G. Hamidani, D. R. Krützfeldt, and T.
Flavus for their technical assistance in the behavioural
experiments; M. Weissburg for use of his flume at Georgia
Institute of Technology and T. Keller for advice and
assistance in the flume studies; P. Harrison for helpful
discussions; and the staff of the Keys Marine Laboratory,
Long Key, Florida, USA, for supplying lobsters. This
material was based on work supported by the National
Science Foundation under Grant IBN-0077474, the National
Institutes of Health under Grant DC00312, and the Georgia
Abramson, C. I., and Feinman, R. D. (1990). Operant conditioning in
crustaceans. In ‘Frontiers in Crustacean Neurobiology’. (Eds K.
Wiese, W. -D. Krenz, J. Tautz, H. Reichert, and B. Mulloney.) pp.
207–14. (Birkhäuser: Basel.)
Ache, B. W. (1989). Central and peripheral bases for mixture
suppression in olfaction: a crustacean model. In ‘Perception of
Complex Smells and Tastes’. (Eds D. G. Laing, W. S. Cain, R. L.
McBride, and B. W. Ache.) pp. 101–14. (Academic Press: Sydney.)
Ache, B. W. (1991). Phylogeny of smell and taste. In ‘Smell and Taste
in Health and Disease’. (Eds T. V. Getchell, R. L. Doty, L. M.
Bartoshuk, and J. B. Snow, Jr.) pp. 3–18. (Raven Press: New
Ache, B. W., and Zhainazarov, A. B. (1995). Dual second-messenger
pathways in olfactory transduction. Current Opinions in
Neurobiology 5, 461–66.
Atema, J. (1995). Chemical signals in the marine environment:
dispersal, detection, and temporal signal analysis. Proceedings of
the National Academy of Sciences of the United States of America
Atema, J. (1996). Eddy chemotaxis and odor landscapes: exploration
of nature with animal sensors. Biological Bulletin (Woods Hole)
Atema, J., Borroni, P. F., Johnson, B. R., Voigt, R., and Handrich, L.
(1989). Adaptation and mixture interactions in chemoreceptor
cells: mechanisms for diversity and contrast enhancement. In
‘Perception of Complex Smells and Tastes’. (Eds D. G. Laing, W.
S. Cain, R. L. McBride, and B. W. Ache.) pp. 83–100. (Academic
Bleckmann, H., Breithaupt, T., Blickhan, R., and Tautz, J. (1991). The
time course and frequency content of hydrodynamic events caused
by moving fish, frogs, and crustaceans. Journal of Comparative
Physiology A 168, 749–57.
Breithaupt, T., and Tautz, J. (1990). The sensitivity of crayfish
mechanoreceptors to hydrodynamic and acoustic stimuli. In
‘Frontiers in Crustacean Neurobiology’. (Eds K. Wiese, W. -D.
Krenz, J. Tautz, H. Reichert, and B. Mulloney.) pp. 114–20.
1348 Charles D. Derby et al.
Caldwell, R. L., and Dingle, J. (1985). A test of individual recognition
in the stomatopod Gonodactylus festae. Animal Behaviour 33, 101–
Carr, W. E. S. (1988). The molecular nature of chemical stimuli in the
aquatic environment. In ‘Sensory Biology of Aquatic Animals’.
(Eds J. Atema, R. R. Fay, A. N. Popper, and W. N. Tavolga.) pp. 3–
27. (Springer-Verlag: New York.)
Carr, W. E. S., Gleeson, R. A., and Trapido-Rosenthal, H. G. (1990).
The role of perireceptor events in chemosensory processes. Trends
in Neuroscience 13, 212–15.
Cate, H. S., and Derby, C. D. (2000). A chemo-mechanosensillum that
is ubiquitous on the Caribbean spiny lobster and other lobster
species. Society for Neuroscience Abstracts 30, 66. 16.
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
and Tissue Research 304, 439–54.
Cromarty, S. I., and Derby, C. D. (1998). Inhibitory receptor binding
events among the components of complex mixtures contribute to
mixture suppression in responses of olfactory receptor neurons of
spiny lobsters. Journal of Comparative Physiology A 183, 699–
Daniel, P. C., and Derby, C. D. (1988). Behavioral olfactory
discrimination of mixtures in the spiny lobster (Panulirus argus)
based on a habituation paradigm. Chemical Senses 13, 385–95.
Daniel, P. C., Burgess, M. F., and Derby, C. D. (1996). Responses of
olfactory receptor neurons in the spiny lobster to binary mixtures
are predictable using a noncompetitive model that incorporates
excitatory and inhibitory transduction pathways. Journal of
Comparative Physiology A 178, 523–36.
Derby, C. D. (1989). Physiology of sensory neurons in
morphologically identified cuticular sensilla of crustaceans. In
‘Functional Morphology of Feeding and Grooming in Crustacea’.
(Eds B. E. Felgenhauer, L. Watling, and A. B. Thistle.) pp. 27–47.
(A. A. Balkema: Rotterdam.)
Derby, C. D. (2000). Learning from spiny lobsters about
chemosensory coding of mixtures. Physiology and Behavior 69,
Derby, C. D., and Atema, J. (1981). Selective improvement in
responses to prey odors by the lobster, Homarus americanus,
following feeding experience. Journal of Chemical Ecology 7,
Derby, C. D., and Atema, J. (1982). The function of chemo- and
mechanoreceptors in lobster (Homarus americanus) feeding
behaviour. Journal of Experimental Biology 98, 317–27.
Derby, C. D., and Atema, J. (1988). Chemoreceptor cells in aquatic
invertebrates: peripheral filtering mechanisms in decapod
crustaceans. In ‘Sensory Biology of Aquatic Animals’. (Eds J.
Atema, R. R. Fay, A. N. Popper, and W. N. Tavolga.) pp. 365–88.
(Springer: New York.)
Derby, C. D., Girardot, M. -N., Daniel, P. C., and Fine-Levy, J. B.
(1989). Olfactory discrimination of mixtures: behavioral,
electrophysiological and theoretical studies using the spiny lobster
Panulirus argus. In ‘Perception of Complex Smells and Tastes’.
(Eds D. G. Laing, W. S. Cain, R. L. McBride, and B. W. Ache.) pp.
65–82. (Academic Press: Sydney.)
Devine, D. V., and Atema, J. (1982). Function of chemoreceptor
organs in spatial orientation of the lobster, Homarus americanus:
differences and overlap. Biological Bulletin (Woods Hole) 163,
Feinman, R. D., Abramson, C. I., and Forman, R. R. (1990). Classical
conditioning in the crab. In ‘Frontiers in Crustacean
Neurobiology’. (Eds K. Wiese, W. -D. Krenz, J. Tautz, H. Reichert,
and B. Mulloney.) pp. 215–22. (Birkhäuser: Basel.)
Fine-Levy, J. B., and Derby, C. D. (1991). Effects of stimulus intensity
and quality on discrimination of odorant mixtures by spiny lobsters
in an associative learning paradigm. Physiology and Behavior 49,
Fine-Levy, J. B., Girardot, M. -N., Derby, C. D., and Daniel, P. C.
(1988). Differential associative conditioning and olfactory
discrimination in the spiny lobster Panulirus argus. Behavioral and
Neural Biology 49, 315–31.
Fine-Levy, J. B., Daniel, P. C., Girardot, M. -N., and Derby, C. D.
(1989). Behavioral resolution of quality of odorant mixtures by
spiny lobsters: differential aversive conditioning of olfactory
responses. Chemical Senses 14, 503–24.
Girardot, M. -N., and Derby, C. D. (1988). Neural coding of quality of
complex olfactory stimuli in lobsters. Journal of Neurophysiology
Girardot, M. -N., and Derby, C. D. (1990a). Independent components
of the neural population response for discrimination of quality and
intensity of chemical stimuli. Brain, Behavior and Evolution 35,
Girardot, M. -N., and Derby, C. D. (1990b). Peripheral mechanisms of
olfactory discrimination of complex mixtures by the spiny lobster:
no cell types for mixtures but different contributions of the cells to
the across neuron patterns. Brain Research 513, 225–36.
Gleeson, R. A. (1991). Intrinsic factors mediating pheromone
communication in the blue crab, Callinectes sapidus. In
‘Crustacean Sexual Biology’. (Eds R. T. Bauer and J. W. Martin.)
pp. 17–32. (Columbia Univ. Press: New York.)
Gleeson, R. A., Carr, W. E. S., and Trapido-Rosenthal, H. G. (1993).
Morphological characteristics facilitating stimulus access and
removal in the olfactory organ of the spiny lobster, Panulirus
argus: insight from the design. Chemical Senses 18, 67–75.
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. Journal of
Comparative Physiology A 185, 427–36.
Grasso, F. W., Basil, J. A., and Atema, J. (1998a). Toward the
convergence: robot and lobster perspectives of tracking odors to
their source in the turbulent marine environment. In ‘Proceedings,
1998 IEEE/RSJ International Conference on Intelligent Robots and
Systems: Innovations in Theory, Practice and Applications,
October 13–17, 1998, Victoria Conference Centre, Victoria, B. C.,
Canada.’ pp. 259–64. (Institute of Electrical and Electronics
Engineers: Piscataway, New Jersey, USA.)
Grasso, F. W., Basil, J. A., and Atema, J. (1998b). Roles of lateral
antennule chemo- and mechano-sensation on the chemo-orientation
in the American lobster (Homarus americanus). The Fifth
International Congress of Neuroethology (San Diego, CA; August
23–28, 1998). Abstract #157.
Grasso, F. W., Consi, T. R., Mountain, D. C., and Atema, J. (1999).
Biomimetic robot lobster performs chemo-orientation in turbulence
using a pair of spatially separated sensors: progress and challenges.
Journal of Robotics and Autonomous Systems 807, 1–17.
Grünert, U., and Ache, B. W. (1988). Ultrastructure of the aesthetasc
(olfactory) sensilla of the spiny lobster, Panulirus argus. Cell and
Tissue Research 251, 95–103.
Hazlett, B. A. (1994a). Alarm responses in the crayfish Orconectes
virilis and Orconectes propinquus. Journal of Chemical Ecology
Hazlett, B. A. (1994b). Crayfish feeding responses to zebra mussels
depend on microorganisms and learning. Journal of Chemical
Ecology 20, 2623–30.
Hazlett, B. A., and Schoolmaster, D. R. (1998). Responses of cambarid
crayfish to predator odor. Journal of Chemical Ecology 24, 1757–
Sensory basis of feeding behaviour, P. argus
Hildebrand, J. G., and Shepherd, G. M. (1997). Mechanisms of
olfactory discrimination: converging evidence for common
principles across phyla. Annual Review of Neuroscience 20, 595–
Horner, A. J., Ngo, V., Steullet, P., Keller, T., Weissburg, M. J., and
Derby, C. D. (2000). The role of different types of antennular
sensilla in orientation by Caribbean spiny lobsters to a natural odor
stimulus under controlled flow conditions. Chemical Senses 25,
Johnson, B. R., Voigt, R., Merrill, C. L., and Atema, J. (1992). Across-
fiber patterns may contain a sensory code for stimulus intensity.
Brain Research Bulletin 26, 327–31.
Karavanich, C., and Atema, J. (1998a). Individual recognition and
memory in lobster dominance. Animal Behaviour 56, 1553–60.
Karavanich, C., and Atema, J. (1998b). Olfactory recognition of urine
signals in dominance fights between male lobster, Homarus
americanus. Behaviour 135, 719–30.
Krasne, F. B. (1973). Learning in Crustacea. In ‘Invertebrate Learning.
Vol. 2: Arthropods and Gastropod Mollusks’. (Eds W. C. Corning,
J. A. Dyal, and A. O. D. Willows.) pp. 49–130. (Plenum Press:
Laverack, M. S. (1964). The antennular sense organs of Panulirus
argus. Comparative Biochemistry and Physiology 13, 301–21.
Laverack, M. S. (1988a). The numbers of neurons in decapod
Crustacea. Journal of Crustacean Biology 8, 1–11.
Laverack, M. S. (1988b). The diversity of chemoreceptors. In ‘Sensory
Biology of Aquatic Animals’. (Eds J. Atema, R. R. Fay, A. N.
Popper, and W. N. Tavolga.) pp. 287–312. (Springer-Verlag: New
Livermore, B. A., Hutson, M., Ngo, V., Hadjisimos, R., and Derby, C.
D. (1997). Elemental and configural learning and the perception of
odorant mixtures by the spiny lobster Panulirus argus. Physiology
and Behavior 62, 169–74.
Lynn, W. H., Meyer, E. A., Peppiatt, C. E., and Derby, C. D. (1994).
Perception of odor mixtures by the spiny lobster Panulirus argus.
Chemical Senses 19, 331–47.
McClintock, T. S., Xu, F., Quintero, J., Gress, A. M., and Landers, T.
M. (1997). Molecular cloning of a lobster Gα-q protein expressed
in neurons of olfactory organ and brain. Journal of Neurochemistry
Marschall, H. -P., and Ache, B. W. (1989). Response dynamics of
lobster olfactory neurons during simulated natural sampling.
Chemical Senses 14, 725 (abstract.)
Maynard, D. M. (1966). Integration in crustacean ganglia. Symposium
of the Society for Experimental Zoology 20, 111–49.
Mellon, D., Jr., and Alones, V. (1993). Cellular organization and
growth-related plasticity of the crayfish olfactory midbrain.
Microscopy Research and Technique 24, 231–59.
Merrill, C. L., Voigt, R., and Atema, J. (1994). Reliability of
chemoreceptor cell response. I. Intensity coding by pattern and
response magnitude with a comparison of analytical methods.
Journal of Comparative Physiology A 175, 95–105.
Moore, P., and Atema, J. (1988). A model of a temporal filter in
chemoreception to extract directional information from a turbulent
odor plume. Biological Bulletin (Woods Hole) 174, 355–63.
Moore, P. A., and Grills, J. L. (1999). Chemical orientation to food by
the crayfish Orconectes rusticus: influence of hydrodynamics.
Animal Behaviour 58, 953–963.
Moore, P. A., Scholz, N., and Atema, J. (1991). Chemical orientation
of lobster, Homarus americanus, in turbulent odor plumes. Journal
of Chemical Ecology 17, 1293–307.
Munger, S. D., Gleeson, R. A., Aldrich, H. C., Rust, N. C., Ache, B.
W., and Greenberg, R. M. (2000). Characterization of a
phosphoinositide-mediated odor transduction pathway reveals
plasma membrane localization of an inositol 1,4,5-trisphosphate
receptor in lobster olfactory receptor neurons. Journal of
Biological Chemistry 275, 20450–57.
Olson, K. S., and Derby, C. D. (1995). Inhibition of taurine and 5’
AMP olfactory receptor sites of the spiny lobster Panulirus argus
by odorant compounds and mixtures. Journal of Comparative
Physiology A 176, 527–40.
Pereyra, P., Saraco, M., and Maldonado, H. (1999). Decreased
response or alternative defensive strategies in escape: two different
types of long-term memory in the crab Chasmagnathus. Journal of
Comparative Physiology A 184, 301–10.
Ratchford, S. G., and Eggleston, D. B. (1998). Size- and scale-
dependent chemical attraction contribute to an ontogenetic shift in
sociality. Animal Behaviour 56, 1027–34.
Ratchford, S. G., and Eggleston, D. B. (2000). Temporal shift in the
presence of a chemical cue contributes to a diel shift in sociality.
Animal Behaviour 59, 793–99.
Reeder, P. B., and Ache, B. W. (1980). Chemotaxis in the Florida
spiny lobster, Panulirus argus. Animal Behaviour 28, 831–39.
Rescorla, R. A., Grau, J. W., and Durlach, P. J. (1985). Analysis of the
unique cue in configural discrimination. Journal of Experimental
Psychology 11, 356–66.
Rudy, J. W., and Sutherland, R. J. (1992). Configural and elemental
associations and the memory of coherence problem. Journal of
Comparative Neuroscience 4, 208–16.
Sandeman, D. (1990). Structural and functional levels in the
organization of decapod crustacean brains. In ‘Frontiers in
Crustacean Neurobiology’. (Eds K. Wiese, W. -D. Krenz, J. Tautz,
H. Reichert, and B. Mulloney.) pp. 223–39. (Birkhäuser: Basel.)
Sandeman, D., Sandeman, R., Derby, C., and Schmidt, M. (1992).
Morphology of the brain of crayfish, crabs, and spiny lobsters: a
common nomenclature for homologous structures. Biological
Bulletin (Woods Hole) 183, 304–26.
Sandeman, D. C. (1989). Physical properties, sensory receptors and
tactile reflexes of the antenna of the Australian freshwater crayfish
Cherax destructor. Journal of Experimental Biology 141, 197–217.
Schmidt, M., and Ache, B. W. (1996a). Processing of antennular input
in the brain of the spiny lobster, Panulirus argus. I. Non-olfactory
chemosensory and mechanosensory pathway of the lateral and
median antennular neuropils. Journal of Comparative Physiology A
Schmidt, M., and Ache, B. W. (1996b). Processing of antennular input
in the brain of the spiny lobster, Panulirus argus. II. The olfactory
pathway. Journal of Comparative Physiology A 178, 605–28.
Smith, B. H. (1996). The role of attention in learning about odorants.
Biological Bulletin (Woods Hole) 191, 76–83.
Steullet, P., Flavus, T., Radman, D., Hamidani, G., Zhou, M., Dudar,
O., Hill, R., and Derby, C. D. (1999). The aesthetasc-olfactory lobe
pathway of spiny lobsters is not necessary for odor-activated
searching behavior, odor-associate learning, and discrimination of
complex odors. Chemical Senses 24, 613 (abstract.)
Steullet, P., Cate, H. S., Michel, W. C., and Derby, C. D. (2000a).
Functional units of a compound nose: aesthetasc sensilla house
similar populations of olfactory receptor neurons on the crustacean
antennule. Journal of Comparative Neurology 418, 270–80.
Steullet, P., Kruetzfeldt, D. R., Hamidani, G., Flavus, T., and Derby, C.
D. (2000b). Functional overlap of two antennular chemosensory
pathways in food odor discrimination behavior of spiny lobsters.
Chemical Senses 25, 671 (abstract.)
Tautz, J., and Sandeman, D. C. (1980). The detection of waterborne
vibration by sensory hairs on the chelae of the crayfish. Journal of
Experimental Biology 88, 351–56.
Weissburg, M. J. (1997). Chemo- and mechanosensory orientation by
crustaceans in laminar and turbulent flows: from odor trails to
vortex streets. In ‘Orientation and Communication in Arthropods’.
(Ed. M. Lehrer.) pp. 215–46. (Birkhäuser: Basel.)
1350 Charles D. Derby et al. Download full-text
Weissburg, M. J. (2000). The fluid dynamical context of
chemosensory behavior. Biological Bulletin (Woods Hole) 198,
Weissburg, M. J., and Zimmer-Faust, R. K. (1993). Life and death in
moving fluids: hydrodynamic effects on chemosensory-mediated
predation. Ecology 74, 1428–43.
Weissburg, M. J., and Zimmer-Faust, R. K. (1994). Odor plumes and
how blue crabs use them in finding prey. Journal of Experimental
Biology 197, 349–75.
Wight, K., Francis, L., and Eldridge, D. (1990). Food aversion learning
by the hermit crab Pagurus granosimanus. Biological Bulletin
(Woods Hole) 178, 205–09.
Winn, H. E., and Olla, B. L., Eds (1972). ‘Behavior of Marine
Animals. Vol. 1: Invertebrates.’ (Plenum Press: New York.)
Xu, F., Hollins, B., Landers, T. M., and McClintock, T. S. (1998).
Molecular cloning of a lobster Gβ subunit and Gβ expression in
olfactory receptor neuron dendrites and brain neuropil. Journal of
Neurobiology 36, 525–36.
Zhainazarov, A. B., and Ache, B. W. (1999). Effects of
phosphatidylinositol 4,5-bisphosphate and phosphatidylinositol 4-
phosphate on a Na+-gated nonselective cation channel. Journal of
Neuroscience 19, 2929–37.
Zimmer, R. K., and Butman, C. A. (2000). Chemical signaling
processes in the marine environment. Biological Bulletin (Woods
Hole) 198, 168–87.
Zimmer-Faust, R. K. (1987). Gregariousness and sociality in spiny
lobsters: implications for den habituation. Journal of Experimental
Marine Biological and Ecology 105, 57–71.
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. Biological Bulletin (Woods Hole) 188, 111–16.
Zimmer-Faust, R. K., O’Neill, P. B., and Schar, D. W. (1996). The
relationship between predator activity state and sensitivity to prey
odor. Biological Bulletin (Woods Hole) 190, 82–87.
Zulandt Schneider, R. A., and Moore, P. A. (1999). Recognition of
dominance status through chemoreception in the red swamp
crayfish, Procambarus clarkii. Journal of Chemical Ecology 25,
Zulandt Schneider, R. A., and Moore, P. A. (2000). Urine as a source
of conspecific disturbance signals in the crayfish Procambarus
clarkii. Journal of Experimental Biology 203, 765–71.