Mar. Freshwater Res.

,

2001,

52

,

1339–50

© CSIRO 2001 10.1071/MF01099 1323-1650/01/081339

The sensory basis of feeding behaviour in the Caribbean spiny lobster,

Panulirus argus

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: cderby@gsu.edu

Abstract.

A complex nervous system enables spiny lobsters to have a rich behavioural repertoire. The presentpaper discusses the ways in which the sensory systems of the Caribbean spiny lobster,

Panulirus

argus

,particularly its chemosensory systems, are involved in feeding behaviour. It addresses the neural mechanisms ofthree aspects of their food-finding ability: detection, identification, and discrimination of natural food odours; theeffect of learning on responses to food odours; the mechanisms by which spiny lobsters orient to odours from adistance 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 byexperience, including associative and nonassociative conditioning; that spiny lobsters can readily orient to distantodour sources; and that both chemo- and mechanosensory antennular input are important in this behaviour. Eitheraesthetasc or nonaesthetasc chemosensory pathways can be used in identifying odour quality, mediating learnedbehaviours, and permitting orientation to the source of distant odours. Studying the neuroethology of feedingbehaviour helps us understand how spiny lobsters are adapted to living in complex and variable environments.

Extra

keywords

:

Crustacea, olfaction, chemical sense, chemoreception, mechanoreception, orientation,

discrimination, learning

Introduction

The nervous system of spiny lobsters contains an enormousnumber and diversity of neurons. For example, receptorneurons number well over 1 million (Grünert and Ache1988; Laverack 1988

a

; Cate and Derby, 2000, 2001), andthe brain has many sensory and integrative centres, eachwith a different, complex organization (Maynard 1966;Sandeman 1990; Sandeman

et

al

. 1992; Mellon and Alones1993; Schmidt and Ache 1996

a

, 1996

b

). These animals alsoperform a rich array of behaviours, show extensivebehavioural plasticity, and have impressive learningabilities (Winn and Olla 1972; Krasne 1973; Abramson andFeinman 1990; Feinman

et

al

. 1990; Pereyra

et

al

. 1999;Derby 2000). Studying their nervous system andbehavioural abilities, and the causal links between the two,gives us a better understanding of how spiny lobsters andother crustaceans have adapted to living in complex andvariable environments.

The chemosensory pathways are a prominent part of thenervous system of spiny lobsters and other crustaceans. Thefirst antennae (antennules) alone have over 500,000chemosensory neurons (Grünert and Ache 1988; Steullet

etal

. 2000

a

; Cate and Derby 2001), and six paired neuropils

(olfactory lobes, lateral antennular neuropils, medianantennular neuropils, accessory lobes, terminal medullae,and hemiellipsoid bodies) are directly or indirectlyconnected to this antennular input (Sandeman

et

al

. 1992;Schmidt and Ache 1996

a

, 1996

b

).It is therefore not surprising that spiny lobsters use their

chemical senses in many behaviours, including feeding(Reeder and Ache 1980; Zimmer-Faust

et

al

. 1996) andshelter selection (Ratchford and Eggleston 1998, 2000;Zimmer-Faust 1987). Whether they also use their chemicalsenses in larval settlement, avoiding predators, mateselection, social interactions among conspecifics, or otherintra- and interspecific interactions remains to bedetermined, a l though these funct ions have beendemonstrated in other crustaceans (Caldwell and Dingle1985; Carr 1988; Gleeson 1991; Hazlett 1994

a

; Hazlett andSchoolmaster 1998; Karavanich and Atema 1998

a

, 1998

b

;Zulandt Schneider and Moore 1999, 2000). Feedingbehaviour is the best studied of the chemosensorybehaviours in spiny lobsters, especially in terms of sensorymechanisms. The present paper summarizes our currentunderstanding of this topic.

1340 Charles D. Derby

et al.

To use its chemical senses to find food, an animal mustsuccessfully perform several tasks involving sensory,integrative, and motor functions. First, it must identify thenature of the chemical signals. It must detect and distinguishrelevant chemical signals against background chemicals,and it must determine the qualities (

i

.

e

., molecularstructures), quantities (

i

.

e

., concentrations), and locations(

i

.

e

., spatiotemporal dynamics) of these signals. Second, itmust decide whether or not to search for the sources of thosesignals. To do so, it must compare this chemosensory inputwith innate or learned neural templates and makebehavioural choices whether or not to respond, and if so,how to respond. Third, it must locate the source of thesignals by orienting to them from a distance using availablecues, such as the spatiotemporal distribution of chemicaland hydrodynamic cues.

Here, we review work that shows that spiny lobsters canaccomplish all of these tasks. We focus on the Caribbeanspiny lobster,

Panulirus

argus

, which has been an organismof choice in neurobiological studies of the chemical senses.First, we describe mechanisms of detection, identification,and discrimination of behaviourally relevant chemicalsignals, especially complex food-related mixtures. Second,we show that spiny lobsters can change their responses tochemical signals in adaptive ways, as a result of experiencessuch as associative learning. Third, we explain sensorymechanisms involved in orientation toward distant chemicalsignals under natural flow conditions.

Detection and discrimination of chemical signals

The first tasks that spiny lobsters must accomplish duringfeeding—detecting, identifying, and discriminating thenature of chemical cues—are accomplished through theirimpressive chemosensory systems. Chemical sensors arepresent on most body surfaces, especially the first antennae(= antennules), second antennae, legs, and mouthparts, butalso the cephalothorax, abdomen, and telson (Fig. 1

A

)(Laverack 1964, 1988

b

; Grünert and Ache 1988; Derby1989; Gleeson

et

al

. 1993; Cate and Derby 2000, 2001). Thechemosensors are organized as sensilla, which are cuticularextensions of the body surface that are innervated by thedendrites of chemosensory neurons. The aesthetascs are aprominent type of chemosensor that are located only on thedistal half of the antennular lateral flagella; they are the onlyknown unimodal chemosensors (Laverack 1964; Grünertand Ache 1988; Derby 1989; Cate and Derby 2001) (Figs1

A

and 1

B

). All of the other known chemosensilla on

P

.

argus

a re b imodal , be ing innervated by bothchemosensory neurons and mechanosensory neurons (Cateand Derby 2000, 2001). These include hooded sensilla (Figs1

C

and 1

D

) and simple sensilla (Figs 1

E

and 1

F

). Thehooded sensilla are a particularly interesting sensillar type,because they are abundantly located over most of theanimal’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 thefeeding behaviour of lobsters: antennular chemoreceptorsinitiate searching and orientation toward the source of adistant chemical stimulus (Reeder and Ache 1980; Devineand Atema 1982; Steullet

et

al

. 2000

b

); leg chemoreceptorscon t ro l loca l g rasp ing re f l exes ; and mouthpar tchemoreceptors mediate the decision to ingest food (Derbyand Atema 1982). The roles of the chemoreceptors on thecephalothorax and abdomen have not been examined.

The neural basis for discrimination of food odours hasbeen extensively studied in the chemosensory neurons of theantennules. The first step in this process—the transductionof chemical information into electrical signals by antennularreceptor neurons—is known in cellular and molecular detailthat reveals the function of receptor proteins, G-proteins,second-messenger cascades, ion channels, transporters, andenzymes in detecting odorant molecules (Carr

et

al

. 1990;Ache and Zhainazarov 1995; Olson and Derby 1995;McClintock

et

al

. 1997; Xu

et

al

. 1998; Zhainazarov andAche 1999; Munger

et

al

. 2000). Beyond chemosensorytransduction, how chemical quality and quantity areencoded by the chemosensory neurons of the antennules hasalso been well studied in lobsters, both the spiny lobster

P

.

argus

and the American lobster

Homarus

americanus

(for reviews, see Atema

et

al

. 1989; Derby

et

al

. 1989;Derby and Atema 1988; Derby 2000). Each antennule hashundreds of thousands of chemoreceptor neurons (Grünertand Ache 1988; Cate and Derby 2000, 2001). The antennuleas a whole is sensitive to many different odorants,particularly to small, water-soluble molecules such as aminoacids, amines, nucleotides, and sometimes sugars andpeptides (Carr 1988). Yet each antennular chemoreceptorneuron responds to a limited subset of these chemicalstimulants. Individual neurons are not specifically tuned torespond to only one complex stimulus; most cells respond todifferent degrees to all tested complex food mixtures(Girardot and Derby 1990

b

). The responsiveness ofindividual neurons to the components of these mixtures isoften complex: typically, each neuron is excited by someodour compounds, is inhibited by others, and givescomplex, nonlinear, often unpredictable responses tocombinations of odour compounds (Ache 1989; Atema

et

al

.1989; Derby

et

al

. 1989; Cromarty and Derby 1998; Derbyand Atema 1988; Derby 2000). Thus, chemoreceptorneurons of spiny lobsters are complex peripheral processingunits.

How then is chemical quality determined? The likelyanswer is ‘across-neuron response patterns’, also called‘distributed’ or ‘ensemble’ neural response patterns. Anacross-neuron pattern distinguishes one odorant fromanother by differences in the relative activity among most orall members of a neuronal population, rather than by the

Sensory basis of feeding behaviour,

P. argus

1341

presence or absence of activity in a specific subset ofspecialized neurons. Support for the idea that the antennularchemosensory system of

P

.

argus

uses across-neuronresponse patterns in quality coding comes from studies ofresponses of receptor neurons to different sets of food-related chemicals, including simple stimuli (singlecompounds), complex artificial stimuli (binary andmulticomponent mixtures), and complex natural stimuli(tissue extracts from potential prey species). Figure 2 showsacross-neuron response patterns for four differentmulticomponent artificial stimuli representing food—crabmixture, shrimp mixture, mullet mixture, and oystermixture. The across-neuron response patterns for thesemixtures are different from each other (Fig. 2

A

), and these

differences are highly correlated with differences in both theanimal’s perceived quality of the mixtures (Fig. 2

B

) and themixtures’ compositions (Fig. 2

C

). Crab mixture and shrimpmixture, which have the most similar compositions amongthese four mixtures, generate the most similar across-neuronresponse patterns and are perceived by lobsters as beingmost similar. Crab mixture and oyster mixture, on the otherhand, have highly dissimilar compositions, evoke highlydifferent across-neuron response patterns, and are perceivedby lobsters as being more dissimilar in quality. Spinylobsters therefore appear to use sensory information in theform of across-neuron response patterns in their antennularchemosensory system to discriminate the quality of natural,complex chemical stimuli.

medial flagellum

lateral flagellum

antennule

antenna

cephalothorax legs

abdomen

aesthetasc tuft

telsonA

F

E

D

C

B

a as

gscs

10 µm

60 µm

5 µm

5 µm

60 µm

Fig. 1.

Sensors on the Caribbean spiny lobster,

Panulirus

argus

. (

A

) Chemo- and mechanosensors are ubiquitous on the body andappendages, including both flagella of the first antennae (antennules), second antennae, mouthparts, legs, cephalothorax, abdomen, andtelson. Modified from Grünert and Ache (1988). (

B

) Scanning electron micrograph of the distal region of the lateral flagellum of theantennule, showing some of the setae unique to this region: aesthetasc sensilla (a), guard setae (gs), companion setae (cs), and asymmetricsetae (as). (

C–D

) Hooded sensilla, which are bimodal (chemo-mechano) sensors found on most body surfaces; examples shown here arefrom the cephalothorax (

C

) and the antennular lateral flagellum (

D

). (

E–F

) Simple sensilla, which are bimodal (chemo-mechano) sensorsfound on most body surfaces; examples shown here are a medium simple sensillum (

E

) and a long simple sensillum (

F

) on the antennule.

1342 Charles D. Derby

et al.

(A) Neural Distributed Codes

(B) Behavioral Discrimination

(C) Composition

Fig. 2. Spiny lobsters might use across-neuron response patterns to assess differences in stimulus quality of four complex food-related chemicalmixtures. 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 fromrepresentative species (Carr 1988). (A) Relative similarities between mixtures according to across-neuron response patterns for a population of 30receptor 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 mixturesat 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 similaritybetween the across-neuron pattern responses of these 30 cells to each pair of mixtures was quantified by means of squared Euclidean distances; thispairwise analysis for all pairs of stimuli resulted in a 12 × 12 matrix of similarity measures. This matrix was then applied to multidimensionalscaling, 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, asin all multidimensional scaling, the dimensions do not have ‘labels’. In this figure, each point represents the across-neuron response pattern for onestimulus (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 eachmixture (for C, this is the stimulus space represented by 5–500 µM crab mixture). In this figure, the distance between stimuli or stimulus space iscorrelated with the similarity in across-neuron response patterns; thus, stimuli close to each other have relatively similar across-neuron responsepatterns, and stimuli distant from each other have relatively dissimilar across-neuron response patterns. Thus, this figure shows that the stimulusspace (and therefore across-neuron pattern responses) for crab mixture is relatively similar to that for shrimp mixture but relatively dissimilar to thatfor 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), andoyster mixture (OM), each at two concentrations (50 and 500 µM). The data were collected from four groups of three animals; members of eachgroup were aversively conditioned to both concentrations of a single mixture before generalization testing for the other three mixtures. Behaviouralresponses were ‘aversion values’, based on changes in appetitive and aversion responses due to aversive conditioning. Aversive conditioningfollowed by generalization testing is a standard procedure for determining discrimination abilities of animals. In this analysis, similarities in theaversion values were determined for each pair of stimuli by means of Euclidean distances, and these similarities were used to construct an 8 × 8matrix. 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 thisfigure do not have labels, as explained above under Fig. 2A. In this two-dimensional solution, distances between the stimuli are correlated withperceptual 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 shrimpmixture, but relatively different from oyster mixture or mullet mixture. From Fine-Levy et al. (1989). (C) Relative similarities in the chemicalcompositions of the mixtures. A cluster analysis, which is another type of multivariate analysis, was used to evaluate similarities in the chemicalcompositions 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 matrixof these similarity values was created and used in the cluster analysis, the results of which are depicted as a dendrogram. Mixtures joined at a shortcluster distance have more similar compositions than do mixtures joined at longer distances. Thus, crab and shrimp mixtures have compositionsrelatively similar to each other but different from oyster or mullet mixtures. Only four points appear in this figure, compared to the 12 points in Figs2A and 2B, because the multivariate analysis using Pearson correlation coefficients shows that three concentrations for each mixture type areidentical. From Fine-Levy et al. (1988).

Sensory basis of feeding behaviour,

P. argus 1343

Chemical concentration can be encoded by the overallintensity of responses of the antennular chemoreceptor cells(reviewed by Derby and Atema 1988; Ache 1989; Derby etal. 1989; Derby 2000). An independence of codes forchemical type and quantity would allow constancy in theperceived quality of an odour in spite of the largefluctuations in concentrations that occur in nature. Supportfor this independence in P. argus comes from threeobservations. First, the mean response from a population ofantennular chemoreceptor neurons is highly correlated withstimulus concentration (Girardot and Derby 1988, 1990a;Daniel et al . 1996). Second, changes in st imulusconcentration by as much as two orders of magnitude have arelatively small effect on the across-neuron responsepatterns for stimulus quality (Fig. 2A) (Girardot and Derby

1990a). Third, behavioural discriminations of chemicalquality are relatively insensitive to changes in chemicalintensity (Fig. 2B) (Fine-Levy et al. 1989; Fine-Levy andDerby 1991). An alternative theory of coding of stimulusquality has been proposed for H. americanus: that bothchemical concentration and quality are encoded by across-neuron response patterns (Johnson et al. 1992; Merrill et al.1994).

Whereas across-neuron response patterns are probablyused by spiny lobsters in encoding the quality of food-associated chemicals, other chemical signals, such aspheromones, might be encoded differently. In manyanimals, pheromones are encoded by specialized receptorneurons, which function as ‘labelled lines’ rather than inacross-neuron response patterns (Ache 1991, Hildebrand

% D

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Intact LobstersAesthetasc-ablated LobstersNonaesthetasc-ablated Lobsters

Crab InverseCrab

Shrimp Mullet

% D

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99.9:0.1 99:1 90:10 50:50

Blends of AMP:taurine (x 10-2 mM)

Intact LobstersAesthetasc-ablated Lobsters

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 aresufficient 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 (crabmixture 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 atotal of 10 groups, each consisting of 10–20 animals. In (A), animals were subjected to generalization conditioning; that is, during theconditioning phase, only one mixture, crab mixture, was presented, and it was always paired with the aversive stimulus. In (B), animals weresubjected 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: thecomponent in inverse crab with the highest concentration is the component in crab with the lowest concentration; the component in inverse crabwith the second highest concentration is the component in crab with the second lowest concentration; and so forth, until the component ininverse crab with the lowest concentration is the component in crab with the highest concentration. The ability of animals to learn theconditioned task is quantified in the ordinate, which shows the relative difference between responses of conditioned and unconditioned animalsto 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 theconditioned and unconditioned stimuli (i.e., perception by lobsters of some similarity between the two stimuli) is indicated by a negative valuefor the unconditioned stimulus; and (3) ability to discriminate between conditioned and unconditioned stimuli is indicated by a significantdifference between their ordinal values. Thus, learning of the conditioned mixture is demonstrated for all three groups of animals in (A) andboth 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 candiscriminate between the conditioned and unconditioned mixtures in both (A) and (B), as demonstrated by the difference in values between theconditioned mixtures and the unconditioned ones. Third, in (A) intact animals were better at discriminating between the conditioned andunconditioned 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 difficultdiscriminations (i.e., between different blend ratios of the same binary mixture).

1344 Charles D. Derby et al.

and Shepherd 1997). Neural processing of pheromones hasscarcely been studied in crustaceans, particularly thedecapods, because the molecular identity of theirpheromones is largely unknown (Gleeson 1991).

Antennular chemoreceptors provide the input that leadsto initial discrimination of stimuli and the decision whetheror not to initiate a search (Reeder and Ache 1980; Devineand Atema 1982), but the antennules bear many setal types(Fig. 1), including setae that are known to be innervated andare therefore called ‘sensilla’. Antennular chemosensillainclude aesthetascs, hooded sensilla, and several types ofsimple sensilla (Laverack 1964; Grünert and Ache 1988;Cate and Derby 2000, 2001). Other setae, whose innervationhas not been studied, include guard setae, companion setae,asymmetric setae, and plumose setae. Here we collectivelyca l l a l l an tennula r se tae o ther than aes the tascs‘nonaesthetasc setae’.

The identity of the setal types responsible for antennule-mediated odour discrimination is not obvious anddetermining it requires experimental manipulation. Weexamined this issue by studying the behaviour of spinylobsters in which specific antennular setal types (such asaesthetasc sensilla, nonaesthetasc setae, all antennular setae)had been deafferented and comparing the behaviours ofthese ablated animals with those of control animals that hadreceived no surgical treatment. We examined behaviouraldiscrimination by aversively conditioning lobsters to avoidpreviously stimulatory chemicals and subsequently testingtheir generalization to other chemical stimuli (Steullet et al.1999, 2000b). Intensity of response to odours was quantifiedas the duration of searching behaviour. Results showed thatantennular chemoreceptors are important for evoking thesesearching behaviours, because animals without themresponded significantly less than intact animals. Animalsfrom which either the aesthetasc or nonaesthetasc setae hadbeen removed still responded to the mixtures, learned theconditioning task, and discriminated between theconditioned and nonconditioned mixtures (Fig. 3), soaesthetasc chemoreceptors are sufficient but not necessaryfor lobsters to discriminate between highly related chemicalmix tu r e s . L ikewi se nonaes the t a sc an t ennu l a rchemoreceptors are sufficient but not necessary. We haveobserved the same results under a variety of experimentalconditions. These include using two stimulus sets—a set ofmulticomponent artificial food mixtures (Fig. 3A) and a setof binary mixtures containing the same components(adenosine-5’-monophosphate and taurine) but at differentblend ratios (from 99.9:0.1 to 50:50) (Fig. 3B)—and usingtwo training and discrimination tasks—generalizationconditioning (Fig. 3A) and discrimination conditioning (Fig.3B). Together, these experiments show that there is overlapin the function of the aesthetasc and nonaesthetasc receptorneurons in chemical discrimination, and this overlapfunctions in different biological contexts. There may be

differences in the discriminations mediated by theaesthetasc and nonaesthetasc systems of spiny lobsters, suchas in their responsiveness to social or sex pheromones, butthese differences have not yet been identified.

Learning about chemical signals

After identifying a chemical signal, a lobster must decidewhether to search for its source. In this respect, lobstersshow impressive behavioural plasticity; experience andlearning are important. This plasticity is expected from andbeneficial to animals such as lobsters that can live for manyyears, are omnivorous, live in many different environments,and consequently are exposed to different chemical stimulithat can assume of variety of meanings.

An example of plasticity in chemical responsiveness isthat the hedonic value of food can be modified byexperience. Spiny lobsters can learn through negativeconditioning to avoid naturally attractive chemicals, andthey can learn through positive conditioning to increasetheir attraction to other food-related chemicals. Forexample, as described in the previous section onchemosensory discrimination, spiny lobsters can beassociatively conditioned to stop responding to food odoursthat are normally excitatory and attractive if those stimuliare paired with aversive stimuli (Fine-Levy et al. 1988,1989; Lynn et al. 1994; Livermore et al. 1997). We used asthe aversive unconditioned stimulus a ‘pseudopredator’ (ablack object moved rapidly toward the animal) to simulatenatural conditions, such as a situation where lobsters areattracted to food odours but while searching are chased by apredator. The rapid learning of this conditioning task (5–10trials) and its several-day duration, together with our failuresto condition animals with unnatural aversive stimuli such aselectric shock (Fine-Levy et al. 1988), show that this is apowerful and biologically relevant form of learning. Spinylobsters can also learn by habituation to stop responding topreviously attractive food chemicals (Daniel and Derby1988). Such nonassociative learning requires many trials,however, presumably because food chemicals are normallyhighly attractive and have positive hedonic values, and it istherefore not adaptive for animals to habituate quickly toinnately positive stimuli that have not received concomitantnegative reinforcement.

Spiny lobsters can learn different features of food-relatedcomplex chemical cues, depending on the context oflearning and the available cues. A mixture might beperceived either as a combination of its individualcomponents (i.e., elemental cues) or as a mixture-uniquestimulus (i.e., configural cue). Which of these cuesdominates perception is influenced by the salience of each,including past experience with mixtures and theircomponents. Spiny lobsters are able to learn to respond toeither 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 1345

1985; Rudy and Sutherland 1992; Smith 1996). This abilityhighlights the sophistication of chemosensory processingand learning by lobsters.

Other interest ing forms of learning have beendemonstrated in some crustacean species but not in spinylobsters. These include one-trial food-aversion learning(Wight et al. 1990), learned preferences for the odour ofexperienced foods (Derby and Atema 1981; Hazlett 1994b),learning of the identity of individual conspecifics ordominance status during social encounters (Caldwell andDingle 1985; Hazlett 1994a; Hazlett and Schoolmaster1998; Karavanich and Atema 1998a, 1998b, ZulandtSchneider and Moore 1999, 2000), and other learnedbehaviours (Winn and Olla 1972; Krasne 1973; Abramson

and Feinman 1990; Feinman et al. 1990; Pereyra et al.1999).

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 flumethat produces controlled flow conditions mimicking thosefound in nature (Fig. 4A) (Horner et al. 2000). This studyshows that spiny lobsters can efficiently and reliably orientto odour sources 2 m away (Figs 4B and 5). Similar abilitieshave also been demonstrated in other crustaceans, includingAmerican 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 aesthetascsablated (n = 10)

D. Orientation paths of lobsters with non-aesthetasc chemoreceptors ablated (n = 4)

C. Orientation paths of lobsters with non-aesthetascchemo- and mechanoreceptors ablated (n = 5)

CageStimulus

5 cm/sec75 cm

200 cm

Sea Water5 cm/sec

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 GeorgiaInstitute of Technology. The chemical stimulus was 3 gm/L shrimp extract released by a peristaltic pump at 5 cm/s, which is the same velocityat 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 trialconsisted of placing an animal in the cage, releasing an odour from the source, and videotaping the behavioural response for 10 min with aCCD camera above the flume. (B–E) Orientation paths of individual animals from four treatment groups. The videotaped movements of eachlobster that successfully found the odour source were later digitized and plotted with Motion Analysis® software. The number of individualorientation tracks, each from a different lobster, is shown on each figure for each treatment group. (B) Intact animals: Animals with noablations. (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 antennularnonaesthetasc setae were surgically ablated and/or covered with cyanoacrylate glue; aesthetasc chemoreceptors were intact. (E) Animals withnonaesthetasc chemoreceptors ablated: all antennular nonaesthetasc chemoreceptors were ablated through shaving and gluing ofnonaesthetasc 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 functionalnonaesthetasc chemoreceptors but have functional nonaesthetasc mechanoreceptors as well as aesthetasc chemoreceptors.

1346 Charles D. Derby et al.

Zimmer-Faust et al. 1995), and crayfish (Moore and Grills1999; T. Breithaupt, pers. comm.).

What receptors are used in chemo-orientation oflobsters? The importance of antennules in odour orientationhas been previously demonstrated in both P. argus (Reederand Ache 1980) and H. americanus (Devine and Atema1982; Grasso et al. 1998a), but the antennules have manydifferent setal types, including unimodal chemosensilla(aesthetascs), bimodal chemomechanosensilla (hoodedsensilla and simple sensilla), and many others (Fig. 1).Which of these setae are responsible for chemicalorientation is not known, although the prominentaesthetascs are often assumed to be the mediators. Westudied orientation of animals from which various types ofsetae had been eliminated (Horner et al. 2000) (Figs 4 and5). Intact animals readily initiated searching (i.e., left thecage shelter), usually found the odour source, and did so

rapidly via a direct path (Figs 4B and 5). Animals withoutany functional antennular chemoreceptors but with intactantennular mechanoreceptors (i.e., ‘aesthetasc andnonaesthetasc chemoreceptors ablated’ in Fig. 5A) onlyoccasionally initiated a search and located the source in only1 of 17 trials (Fig. 5), supporting the importance ofantennular chemoreceptors to this behaviour. Animals in allother treatment groups found the odour source withapproximately the same probability. Animals withaesthetascs ablated (Figs 4C and 5) and animals withantennular nonaesthetasc chemoreceptors ablated (Figs 4Dand 5) showed similar behaviour. Both groups were as likelyas intact animals to locate the odour source (Fig. 5A), butsearch efficiency was slightly poorer in these two groupsthan in intact animals—their paths to the odour source weremore circuitous, and the total search time was longer.Interestingly, animals lacking only antennular nonaesthetasc

1.0

0.8

0.6

0.4

0.2

0.0n = 10 n = 4n = 14 n = 4

100

80

60

40

20

0

n = 21 n = 8n = 14 n = 6 n = 17

Percentage of Animals Locating the Odor Source

A. Net-to-Gross Displacement RatioB.

Time to Locate the Odor Source

140

120

100

80

60

40

20

0n = 15 n = 6n = 10 n = 4

C. Control

Aesthetascs Ablated

Non-aesthetasc Chemo- and Mechanoreceptors Ablated

Non-aesthetasc Chemoreceptors Ablated

Aesthetasc and Non-aesthetasc Chemoreceptors Ablated

Fig. 5. Effects of ablations of antennular setae on orientation of spiny lobsters to odours. These figures are based on the data from theorientation tracks in Fig. 4. Sample size for each treatment group is shown in the corresponding panel. Treatments are as in Fig. 4, except alsoshown in (A) are results for animals with ‘aesthetasc and nonaesthetasc chemoreceptors ablated’. This group had both the lateral and medialflagella 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 animalslocating 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 odoursource to the total distance travelled by the animal. A value of one is a direct track to the source, and values approaching zero representincreasingly 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 1347

chemoreceptors (‘nonaesthetasc chemoreceptors ablated’:Figs 4E and 5) were better at orienting than were animalslacking both nonaesthetasc chemo- and mechanoreceptors(Figs 4D and 5). This result points to the importance ofantennular mechanoreceptors to orientation to odours inflow.

Taken together, our results on P. argus suggest thatantennules are necessary for initiating and probably formaintaining searching for distant odours and that bothantennular chemoreceptors and mechanoreceptorscontribute. The setae that mediate this behaviour aredistributed and diverse, because chemoreceptors in eitheraesthetasc or nonaesthetasc setae are sufficient but notnecessary for successful orientation behaviour. Antennularmechanoreceptors contribute to orientation to odours,presumably by providing information about flow cues. Thephysiology of the antennular neurons involved in orientationto distant chemical signals under natural flow conditions isbeginning to be understood, including their ability to resolvethe spatiotemporal distribution of chemical and mechanicalflow cues. Lobster antennular receptor neurons can followchemical stimulus pulses at frequencies as high as fourpulses per second (Marschall and Ache 1989; Gomez et al.1999). These cellular properties allow resolution of thespatiotemporal patterns of chemical signals produced intheir natural environment (Moore and Atema 1988; Atema1995; Weissburg 2000; Zimmer and Butman 2000). Evenbetter studied are assorted sensillar mechanoreceptorneurons, which have response properties that allow them tofollow dynamic changes in water flow under naturalcondit ions, including detect ing the presence andcharacteristics of eddies (Tautz and Sandeman 1980;Sandeman 1989; Breithaupt and Tautz 1990; Bleckmann etal. 1991; Weissburg 1997).

Exactly how chemo- and mechanoreceptors are used incombination in mediating orientation is not known,although several hypotheses based on work on othercrustaceans have been suggested. One proposed mechanism,based on experimental work on the clawed lobster Homarusamericanus, is that animals might orient in and find anodour source using only spatiotemporal features of chemicalcues (Moore and Atema 1988; Moore et al. 1991; Atema1996). This theory has been tested with modelling, robots,and animals (Grasso et al. 1998a, 1998b, 1999), and theresults have generally not supported it but have lead to asecond proposed mechanism—that the spatiotemporald i s t r ibu t ion of no t on ly chemica l cues bu t a l sohydrodynamic cues is used in orientation (Atema 1996;Grasso et al. 1998a, 1999; Moore and Grills 1999). Themechanism might be as relatively simple as an odour-activated rheotaxis, in which odour stimulation initiatessearch while the direction of current flow providesorientation 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 bepresent in the odour-scented eddies themselves that wouldindicate the location of the source (Atema 1996; Grasso eta l . 1998a , 1999; Moore and Gri l l s 1999) . Moreexperimentation is necessary to ascertain whether these orother mechanisms can explain orientation in crustaceans,including P. argus.

Acknowledgments

We thank V. Ngo, G. Hamidani, D. R. Krützfeldt, and T.Flavus for their technical assistance in the behaviouralexperiments; M. Weissburg for use of his flume at GeorgiaInstitute of Technology and T. Keller for advice andassistance in the flume studies; P. Harrison for helpfuldiscussions; and the staff of the Keys Marine Laboratory,Long Key, Florida, USA, for supplying lobsters. Thismaterial was based on work supported by the NationalScience Foundation under Grant IBN-0077474, the NationalInstitutes of Health under Grant DC00312, and the GeorgiaResearch Alliance.

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