Chemical Signal-to-Noise Detection by Spiny Lobsters

8 Pages·1991·3.5 MB·English

by  R K Zimmer-Faust

Reference: Bio/. Bull. 181:419-426. (December, 1991)
Chemical Signal-to-Noise Detection by Spiny Lobsters
RICHARD K. ZIMMER-FAUST*
Marine EnvironmentalSciences Consortium andDepartment ofBiology, University ofAlabama.
P.O. Box 369-370, Dauphin Island, Alabama 36528
Abstract. The smallest difference in concentration de- diate predator-prey interactions (Peckarsky, 1980; Croll,
tected between a chemical stimulus and background is 1983; Zimmer-Faust, 1989; Sih and Moore, 1990), com-
called the threshold of"just noticeable difference" (jnd). petition(Caldwell, 1982; Sammarco<//.. 1983;LaBarre
Measurements ofjnd thresholds have been made exten- et a!.. 1986), courtship and mating (Gleeson et a/.. 1984;
sively in psychophysical research on olfactory and taste Miller, 1989), gregariousness and sociality (Zimmer-Faust
perception by terrestrial mammals, but not on chemo- and Spanier, 1987; Jensen, 1989), and habitat selection
reception by marine organisms. Marine organismslivein (HadfieldandScheuer, 1985; Raimondi, 1988;Sweatman,
apersistently noisychemical environment, because stim- 1988; Morse, 1990). Several properties ofchemical cues,
ulatory compounds are often components of the back- including molecular structure, concentration, and distri-
ground in seawater. Measurements of jnd thresholds, bution in time and space, contribute to the stimulation
therefore, should be especially appropriate in the marine ofa behavioral response.
environmentandwerethefocusofthisstudy. Laboratory The ability to detect concentration differences is es-
assayswereused in measuringtheability ofspiny lobsters, pecially important, because instantaneous or time-aver-
Pamilirusinterruptits. todetect aglycine stimulusagainst aged gradients in chemical concentration may provide
a background concentration ofglycine. Glycine wascho- animals with valuable information about their distance
sen as stimulant because it is a major component ofdis- and direction from the odor source (Moore and Atema,
solved organic matter(DOM) in seawater, isabundant in 1988; Zimmer-Faust el a/., 1988). The source may be
prey tissues, and is excitatory to the appetitive feeding food or a mate, and chemical concentration might also
phase ofP. intemiptus. Chemical determinations ofgly- provide information about the quantity or quality ofthe
cine in seawater were made by reverse-phase, high-per- resource. Becausemanystimulatory moleculesoccurnat-
formance liquid chromatography. Thejndthreshold that urally asdissolved organic matterin seawater, marineor-
wasestimated inthisstudy forglycinedetectionbylobsters ganisms face the problem of resolving chemical signals
was about 2-8% above the background concentration of fromenvironmentalbackground, orchemical "noise." In
glycine in seawater. This threshold is slightly lower than particular, free amino acids, nucleotides, sugars, and or-
onesdemonstrated forodorant detection by humansand ganicacids function assignalsoffood(see reviewsofCarr,
otherterrestrial animals. Consequently, theolfactorysense 1988; Laverack, 1988), but theyalso occurabundantly in
oflobsters appears to be well constructed to detect subtle seawater. The effects ofchemical stimulus concentration
changes between concentrations of stimulus and back- have been considered in many studies on marine animal
ground, a facility that may be important in the ecology behavior(Ache, 1982; Carr, 1988; Zimmer-Faust, 1989),
ofthis animal. but in noinvestigation haveresponsethresholdstoapplied
stimuli been measured relative to background concentra-
Introduction tions. Because manychemoreceptors functionasdetectors
Chemical stimuli are important factors controllingthe ofrelative changes in concentration, threshold determi-
behavior ofaquatic organisms. Chemical cues often me- nations may be products both of animal sensitivity to
tested compounds, and to background chemical levels in
*RePcreeisveendt a1d9drFeesbsr:uaDreypa1r9t9m1e;natccoefptBeidol2o6gySaenpdteMmabreirne199S1c.iences Pro- seaTwhateert.hreshold of "just noticeable difference" (jnd) is
gram. UniversityofSouthCarolina. Columbia. SouthCarolina 29208. thesmallest differencedetected between theconcentration
419
420 R. K. ZIMMER-FAUST
of the stimulus and that of the background. The jnd ments ofwater flow. A secondary flow ( 122 ml/min) was
threshold hasbeen used extensively in psychophysical re- carried by polyethylene tubing from a head-tank to a
search on olfactory and taste perception by vertebrates, stimulus reservoirbefore itjoined the primary flowat the
especially humans(sensit McBurney etal., 1967), but has adaptor. Test stimulant solution was introduced (10 ml/
not been applied to investigations ofchemoreceptive be- 7 s) when a three-way valve that connected the stimulus
havior in marine organisms. Yet measurements ofjnd reservoirto the secondary flow system was opened. A fit-
thresholds should be especially appropriate to marine or- ting in each adaptor eliminated back-flow, ensuring that
ganisms, which live in a persistently noisy chemical en- seawaterand test stimulantswould passfrom the second-
vironment. In fact, thresholddeterminationsofjndshould ary to primary flow before entering a chamber.
be essential to understanding the environmental con-
straintsimposed on chemical detection. Forthese reasons, Choice ofglycine as test stimulus
duringthe present study, analytical procedures useful for
measuringjndthresholds ofchemical detection by marine Glycine was used as test stimulant because it is excit-
organismsweredeveloped. The procedureswerethen ap- atory to the appetitive phase offeeding by P. interruptus
plied in estimating the threshold ofjnd for chemical de- (Zimmer-Faust et al., 1984; Zimmer-Faust, 1987). It is
tection by the spiny lobster, Panulirus inlerruptus. alsoabundant inthetissuesofinvertebratepreyconsumed
by lobsters(e.g.. Bowlus and Somero, 1979; Zurburgand
Materials and Methods DeZwaan. 1981; Yancey et al., 1982) and is released by
some prey as a metabolite (Zimmer-Faust, unpub. data).
Collection andmaintenance of animals Because glycine is one of three most abundant amino
Lobsters were captured by SCUBA divers and were aPcriidtschianrdc,oa1st9a7l8;seGaawrartaesri(eCtlaalr..k 1et98a2l.;. M1o97p2p;eDraawnsdonLianndd-
brought immediately tothe laboratory wheresmallgroups roth, 1982; Fuhrman and Bell, 1985), it isan ecologically
o(1f.i5ndmividdiuaamlestweerreXp0l.a6cemd ihneliagrhgte), ohuavtidnogorecxicrecsuslasrhetlatnekrss dreetleecvtanftrsotmimbualcuksgrmooulnedcunloeisteh.at lobsters must naturally
(see Zimmer-Faust and Spanier, 1987). A continuous
seawater flow (5 ^m filtered) of 8 1/min maintained the
Experimentalprocedures
aeration andtemperature (15-16C)ofeach holdingtank.
Incominganimalsweretattooed on theirventral thoracic Lobsters were placed in experimental chambers 45 to
sternites, permitting individual recognition (Kuris, 1971), 60 min before testing, and they usuallyacclimated within
while gender and reproductivmemstatus were noted. Only 30 min. Observations of behavior were initiated 1 min
hard-shelled animals, 60-69 carapace length, were before the introduction ofa test or control solution and
used in the experiments. All animals were fed adlibitum were continued for 3 min afterwards; the observer was
on live mussels(MytiluscalifornianusandM. edulis), sea unawareofthesolution beingtested. Ineachtrial,alobster
urchins (Strongylocentrotus piirpitratus), and polychaete waspresented with 10 ml ofeithMer 10 :, 10~-\ 10 \ 10 5,
worms (Phragmatopoma californica), but were deprived 10~6, 10~7, 5 X 10~8, or 10~8 glycine added to the
offood for 24 h before testing. seawaterasdescribedabove. Eachconcentration ofglycine
was tested 20 times, each time on a different animal. In
Experimental chambers 40trials, lobsterswere presented onlywith seawater(con-
trol). Each test and control solution was prepared fresh
Individual lobstersweretestedforresponsestochemical immediately priortoassay. Individual lobsters weretested
solutionspresented in rectangularchambers, 30 X 30 X 15 only once in 48 h, for a maximum ofthree times during
cm, constructed soastoallowcareful control ofteststim- an 8-day period. Chemical solutions and their order of
ulus flow characteristics. Opaque blinds around each presentation were selected with a random-numbers table,
chamberpermitted ustoobservethetestanimalswithout except that identical solutions were never repetitively
disturbing them. A diffuse red illumination, completely tested on the same animal.
confined by theblinds, wasprovided, and the surrounding
laboratory was maintained in darkness. Seawater(single- Preparation of chemicalsolutions
pass; 5 nm filtered) entered each chamber by a delivery
system held under constant hydrostatic pressure. Poly- Special carewastaken in preparingtestsolutions. First,
ethylene tubingcarried a primary seawater flow (936 ml/ stocks were made by dissolving glycine in artificial sea-
min) from a head-tank to an adaptor positioned above waterprepared with HPLC-grade DI waterand analytical
each chamber; from the adaptor, the seawater was deliv- gradesaltsaccordingtothe Marine Biological Laboratory
ered tothecenterofthechamber, 0.5 cm belowthewater formula (Cavanaugh, 1975). The concentrations of the
surface. A valve in each delivery line enabled fine adjust- stock solutions were 100-times higher than those ofthe
CHEMICAL SIGNAL-TO-NOISE DETECTION 421
test solutions. Stocks were divided in 1 ml aliquots and brane filters were washed with 10% HC1 (Baker Altrex
frozen at -20C until used. Test solutionswere made by grade), rinsedwith HPLC-grade DI water, and then rinsed
adding 100 ^1 ofan appropriate stock to 9.9 ml seawater; again with sample seawater before use. Chemical deter-
control solutionswere madeby adding 100 n\ ofartificial minations were made by reverse-phase HPLC.
seawater to 9.9 ml seawater. In fact, each solution was Chemical analytical procedures followed those de-
made with seawater drawn from the same experimental scribedpreviously byJones et al. (1981) and Manahan el
chamber that was to be used in the assay. Test concen- al. (1983). Samples were reacted with ortho-phthaldi-
trations, measured by high-performance liquid chroma- aldehyde (OPA) in the presence of mercaptans to form
tography (HPLC) (n = 14 trials), were very accurate and fluorescent products. Sub-samples(100^DofOPA-deriv-
deviated only 2-13% from values estimated volumetri- atives were withdrawn and separated on an Altex ultra-
cally. Glycine concentrations that were maintained in sphere ODS column (150 X 4.6 mm; particle size = 5
chamber seawater did not measurably change duringthe /um; length 15 cm). A gradient was created between two
3-5 min required to prepare a solution (see Results). sodium acetate/methanol buffers (solvent A; 400 ml so-
Consequently, the glycine added with each test solution dium acetate, 95 ml methanol; solvent B: 100 ml sodium
wasan accurate representation ofthe stimulus introduced acetate, 400 ml methanol) (see Jones et al.. 1981), held
above seawater background. at pH 6.8 to improve separation of phenylalanine and
ammonium. Theeluant bufferswere controlled by aGil-
Behavioral assays son (Model 42) gradient analytical system with dual
pumps(Model 302) interfaced with a PC-based program-
Antennule flicking, antennulewiping, legprobing, and ming module (Gilson Model 704). Peaks in the eluant
mouthpart labiating were all used as behavioral assays. stream were monitored with a Gilson (Model 121) fluo-
Both electrophysiological and behavioral investigations rometerand identified by elution time, relativeto known
have shown that flicking is associated with the detection standards. Reagents and solvents all were HPLC grade,
ofchemical stimuli (Snow, 1973; PearsonandOlla, 1977;
degassed prior to use.
Price and Ache, 1977; Pearson el al, 1979; Schmitt and
Ache, 1979; Rebach ct al. 1990). Antennule wiping
against the mouthparts is believed to function either in Determination ofthe ratiometric dilution associated
cleaningorresetting those antennule chemoreceptors that with introduction ofa test stimulus solution
are important to feeding (Snow, 1973; Fuzessery and The dilution associated with stimulus delivery was de-
Childress, 1975). While leg probing is used in contacting termined for a fluorescent dye (sodium fluorescein) in-
foodand passingittothemouth(DerbyandAtema, 1982; troduced in place ofthe test or control solutions (n = 24
Zimmer-Faust and Case, 1982), mouthpart labiating in trials). Fluorescence was monitored with a fast, multi-
preparation foreatingiscarried out with the endopodites channel fluorometer sampling continuously at 10 ms in-
on the third maxillipeds. The following responses arede- tervalsover 3-min trials(Zimmer-Faust etal.. 1988). The
fined: (1) "glycine detection" is an increase in the rate of fluorometerwasequipped with an optical fiberprobe(500
flicking, over 15 sorlonger, within the 3-min test period; yum diameter)placedabout 1 cm belowthepointatwhich
whereas (2) "glycine-mediated appetitive feeding" is the the stimulus entered the test chambers. Optical fibers, as
cmoo-uotchcpuarrrtenlcaebiatoifng,flaillckwiingt,hinwitphien3g-,milnegtestprpoebriinogd.,Thaunds loitghhetrcfolluloercotminegtrdiecvaicneds,spheacvteroaphdoitsotimnecttriacdvmaentthaogdes;oiv.ee.r,
combined, the four acts constitute the initial phases of because flowcellsand pumpingareeliminated, waterflow
feeding (Zimmer-Faust el al, 1984), and they differ isnotdisrupted. Theplacementoftheprobeensuredthat
markedly from the incipient phases of other behaviors, the dye and seawater would be sampled as they entered
suchassocializingandpredatoravoidance(Zimmer-Faust the chambers and before contacting either the olfactory
et al. 1985; Zimmer-Faust and Spanier, 1987). (antennules) or taste (mouthparts, leg tips) organs ofP.
interruptus. Because the dilution of the fluorescein dye
Chemicaldeterminations
was estimated from values determined for peak fluores-
Concentrations ofglycine, ammonium, and 13 other cence, subsequent calculations ofstimulus concentrations
free-amino acids in the seawater sampled from test so- were conservative and probably over-estimated slightly
lutions and experimental chambers were determined. those concentrations actually contacting the sensory ap-
Each aliquot (1 ml) was collected with a polypropylene pendages.
syringe and teflon tubing immediately prior to an exper- The dilution offluorescein dye measured in each trial,
imental test. Samples were filtered gently (<10 psig) to then averaged overall trials, was0.056 (0.1 1 SD) times
0.22 p.m, then placed in cryogenic vials, put on liquid the initial concentration introduced. This value is only
nitrogen, and stored at -76C. All labwares and mem- slightlylowerthan 0.074,which isthedilution, calculated
422 R. K. ZIMMER-FAUST
volumetrically, from the point ofstimulus(anddye) input TableI
to the point ofentry into the experimental chamber, as- Concentrations(nM) ofdissolvedglycine. ammonium, and13other
suming uniform mixing during transport and delivery. freeaminoacidsintheseawaterofexperimentalchambers,
Consequently, volumetric measurements, which are more immediatelybeforestimulusintroduction
easilyobtained, alsoaccuratelyestimate stimulusdilution.
Compound Concentration
Results alanine
Chemicaldeterminations
The glycine concentrations in the seawater ofexperi-
mental chamberswere sampled priorto40selected trials.
Each ofthese trials was chosen at random from among
all ofthose performed, except that determinations were
distributed equally among days. The sources and mag-
nitudes ofwithin-day variation in glycine are difficult to
assess. Duplicateseawatersampleswereoccasionallytaken
atthe sametime from single chambers. Theaverage range
ofglycine concentrations determined from the duplicate
analysesisthe mean 1 1%. While this range seemsrather
large, it is typical of those found by other investigators
that have previously measured free amino acids in sea-
water (e.g., Fuhrman and Bell, 1985). Sixty-five percent
ofthe variance in glycine concentration is explained by
differences occurring between days. The between-day
variation does not differ significantly from the variation
measured within each day (One-way ANOVA: d.f. = 7/
32, F = 1.93, P > 0.10); thus the datajustifiably can be
pooled. Meansand variancesaregiven in Table I forcon-
centrations of glycine, ammonium, and 13 other free
amino acids in the seawater ofexperimental chambers.
Glycine also was measured for seawater drawn each
day from apairofexperimental chambersrandomlycho-
sen, one tank holding a lobster and the other not. Mean
concentrationsintheseawaterofpairedtankswere found
to be nearly equal before, and again 60 min after placing
lobsters (Table II). These data suggest that the glycine
concentrations in seawaterwere stable over intervalsthat
were longerthan the duration ofthe behavioral bioassay.
Nevertheless, small, instantaneous fluctuationsinglycine
mightwell haveoccurredduringtrial intervals. Theeffect
would have been to limit the detection of the glycine
stimulus by the lobsters and to increase the threshold of
jnd proportional to the magnitudes of the fluctuations
(see arguments ofCain, 1977a). Because a very lowjnd
threshold wasdetermined (see next section), it is unlikely
that glycine fluctuated much, ifat all, during the trials.
Ammonium in theseawaterofexperimental chambers
increased significantly when lobsterswerebeing held (Ta-
ble II, and Student's Mest: / = 3.96, d.f. = 14, P < 0.01).
Similarly, concentrations of alanine, aspartic acid, glu-
tamic acid, histidine, and lysine all increased, but to a
lesser extent. Sixty minutes after lobsters were placed in
the seawater, the mean total concentration offree amino
acids was 556 (131 nMSD), as compared to497 (1 10
CHEMICAL SIGNAL-TO-NOISE DETECTION 423
Table II
Concentrations(tM) ofdissolvedglvcine. ammonium, anil 13otherfreeaminoacidsintheseawaterofexperimentalchambers
with lobsterspresentorabsent
Lobsterspresent Lobstersabsent
Compound Time = Time = 60 Time = Time = 60
alanine
424 R. K. ZIMMER-FAUST
ofpeak fluorescence recorded in trials in which dye was delivery ofstimulus solutions to the experimental cham-
released. Consequently, dilution associatedwithstimulus bers, ofthe glycine concentrations in the stimulus solu-
deliverywastheminimumobserved. Second,thethreshold tions, and ofthe glycine concentrations in the seawater
ofjnd is little affected by the method of estimating ra- of the experimental chambers. The threshold determi-
tiometric dilution, whether fluorometric or volumetric. nation was found to be very robust, changing little as a
Substituting a value calculated volumetrically, 0.074, consequenceofvariation in stimulusdilutionandglycine
producesathreshold of/w/thatis2.4%abovebackground. levels.
Third, valuescalculated for H}are very robust. It follows The threshold ofjndreported here for lobsters (2-8%)
from equation 2 that H'f increases as .v increases, as Cc is slightly lower than those (4-33%) found for olfactory
decreases, and as .Y increases, while Cc decreases. Substi- and gustatory detection by terrestrial animals, including
tuting a value of .v two standard deviations above the humans (McBurney et al.. 1967; Shumake el ai, 1969;
mean, while also substituting a value ofCc two standard Pfaffman et ai. 1971; Cain, 1977a, b; Slotnick and Ptak,
deviations below the mean, yields a threshold ofjndthat 1977). Direct chemical measurements ofapplied stimulus
is 8.0% above background. Finally, the duration of in- and background were made in only one ofthese studies
creased antennule flicking was shortened in response to (Cain, 1977a), and backgroundconcentrations fluctuated
the lowest stimulus concentrations tested. For examMple, significantly. Becausetheappliedstimuluswasnotalways
lobsters responded to glycine applied at 5 X 10~8 by maintained above the mean background concentration,
increasingflickingoveronlya20-30sinterval, beginning signal detection theory was used in estimating the likeli-
about 10 s after the initial introduction ofthe stimulus hood of a given difference between stimulus and back-
solution. The onset ofdetection coincided withthe timing ground (Green and Swets, 1974; Egan, 1975). Signal de-
ofpeak fluorescence as measured in trials in which dye tection theory was not required in this study of lobsters
was released. Therefore, the detection ofglycine at low because the applied stimulus was assumed always to be
concentrations ofthisstimulusappears tobe restricted to above background. The application of signal detection
the period during which the level ofintroduced stimulus theory neither increases nor decreases estimates ofjnd
peaks. thresholds, but explains how variation in background
Interestingly, 38% ofall lobsters tested increased their stimuli influences threshold estimates.
antennular flicking in response to seawater(control); i.e., An emerging theme in chemoreception research con-
in the absence ofan applied glycine stimulus (Table III). cernsmechanismsbywhichanimalsdistinguishastimulus
Possibly, thelobstersweredetectingsubstancesintroduced from thebackground noise. Carr(1988) hashypothesized
as contaminants during solution preparation, or issuing that compounds containing novel structural moieties
from other unspecified sources. Alternatively, antennule provide the best chemical cues to marine animals. This
flickingmay havebeen triggeredbysmall changesin water hypothesis isappealingbecause it isadvantageous foran-
flow,orbyairbubblesproducedwhenavalvewasopened imalsto detect signalsthat maximize thecontrast between
and closed during the introduction ofsolutions. To dis- stimulus and background. Alternatively, substances oc-
DOM
tinguish these possibilities, 20 trials were performed in curring as also serve as feeding cues to marine an-
which the valve was opened and then closed without imals(Laverack, 1988). In such instances, thecompounds
stimulus or seawater being introduced. Six ofthe 20 lob- providing the best cues may be those maintained at the
sterstested responded with an increased rateofantennular lowest levels in seawater. Because glycine is abundant in
flicking. The proportion responding(30%) is nearly iden- seawater, yet is an effective stimulus detected by P. inter-
tical to that when the seawater (control) was applied. ruptusat concentrations only slightly above background,
Consequently, increased flicking in response to the sea- the results reported here suggest another alternative. It
water (control) is probably caused by the valve being may be beneficial for animals to maximize differential
opened and closed, not by the lobsters detecting some sensitivityforsignal moleculesthatotherwiselack unique
unidentified, stimulatory compound. structural moieties, but are strongly correlated with a
valuable or limiting resource. Glycine, for example, is
Discussion consistentlyoneofthreeorfourmostabundantfreeamino
acids in marine invertebrate flesh (Carr, 1988), occurring
To my knowledge, this is the first measurement ever at 30-200 mAf. Glycine, therefore, clearly signals the
ofa threshold of"just noticeable difference" for chemo- presence ofpotential prey, because marine invertebrates
reception in an aquaticanimal. Thethreshold concentra- are the principal food resource exploited by lobsters
tion for glycine stimulus detection by the spiny lobster, (Lindberg, 1955).
Panulirm intermptns, is about 2-8% higher than the gly- The mechanism by which lobsters detect small differ-
cine background in seawater. Repeated measurements ences between glycine stimulus and background is un-
were made ofthe ratiometric dilution associated with the known, although sensory adaptation may be involved.
CHEMICAL SIGNAL-TO-NOISE DETECTION 425
Adaptation isachangeinsensitivitytoanappliedstimulus cial thanks go to Dr. M. J. Weissburg and Dr. W. E. S.
resulting from continuous priorexposureto abackground Carr, whose constructive criticisms were essential in de-
stimulus. Stimulusbackgrounds maintained for2-3 min, veloping the manuscript. This project was sponsored by
or longer, are enough to influence the physiological re- grants from the National Science Foundation (Rll-
sponse thresholds ofchemoreceptors on the antennules 8956672), Atlantic Richfield Corporation, and the
of the Florida spiny lobster, Panulirus argus (Trapido- Whitehall Foundation.
Rosenthal et al. 1990). and on the walking legs of the
American lobster, Homarus americanus (Borroni and Literature Cited
Atema, 1988). In both cases, the effect is to mediate a
parallel shift in dose-response functionscorrespondingto Ache. B. VV. 1982. Chemoreception and thermoreception. Pp. 369-
changesintheconcentration oftheadaptingbackground. 398 in The Biology ofCrustacea, Vol. 3. H. L. Atwood and D. C.
Insight may be gained by considering conclusions drawn BorrSoanni,dePm.aFn.,.aendds.J.AAclaedmeam.ic19P8r8e.ss,ANdeawptaYtoirokn.inchemoreceptorcells:
from investigations on vision and hearing. Adaptation is I.Self-adaptingbackgroundsdeterminethresholdandcauseparallel
thought to maintain the auditory and visual senses in shift ofdose-response function. J. Comp. Physiol. A Sens. Neural
working states that allow the detection ofsmall, instan- Behav. Physiol. 164:67-74.
taneous changes in stimulus intensity; i.e., <1% above Bowlus, R. D., and G. N. Somero. 1979. Solute compatibility with
enzymefunctionandstructure: rationalesfortheselectionofosmotic
background (sensu Keidel et al., 1961). In this way, ad- agentsandend-products ofanaerobic metabolism in marine inver-
aptation mayactasan earlyfilter, processinginformation tebrates.J. Exp. Zoo/. 208: 137-153.
andtuninganimal responsestosmall differencesbetween Cain, VV. S. 1977a. Differential sensitivity for smell: "noise" at the
appliedandbackground stimuli. Additional investigation nose. Science195: 796-798.
willclearlybeneededtomorefullyexploretheinteractions Cain,VV.S. 1977b. Odormagnitude:coarsevs. finegrain.Percep. Psy-
between sensory adaptation and chemical detection by Caldcwheolplh,ysR..L2.2:1598425.-549In.terspecificchemicallymediatedrecognitionin
Panulirus interruptus. twocompetingstomatopods. Mar. Behav. Physiol. 8: 189-197.
There is also an urgent need for future investigators of Carr, W. E.S. 1988. The molecularnatureofchemical stimuliinthe
marinechemoreceptive behaviorto measure background aquaticenvironment. Pp. 3-27, in SensoryBiologyofAquaticAni-
stimuli in seawater. Numerous studies have assayed re- mals. J. Atema. R. R. Fay. A. N. Popper, and W. N. Tavolga. eds.
Springer-Verlag, NewYork.
sponses by marine animals, representing nearly every Cavanaugh, G. M. 1975. Formulae and Methods 17 ofthe Marine
majorphylum,toabroadsuiteofstimuli, includingamino Biological Laboratory Chemical Room, 6th ed. Marine Biological
acids, organicacids, sugarsand nucleotidesthat alsooccur Laboratory, Woods Hole.
as DOM (see reviews ofLinstedt, 1971; Carr, 1988; Lav- Clark, M. E., G. A. Jackson, and W. J. North. 1972. Dissolved free
erack, 1988). In several previous studies, the relationship aminoacidsinsouthernCaliforniacoastalwaters. Limnol. Oceanogr.
17: 749-758.
between applied dose and animal response has been ex- Croll,R.P.1983. Gastropodchemoreception.Biol.Rev 58:293-319.
amined, yet in none ofthem were the background levels Dawson, R., and R. G. Pritchard. 1978. The determination ofalpha-
ofstimulant in the seawateroftheexperimental chambers aminoacidsin seawaterusingafluorometricanalyzer. Mar. Chem.
measured. Ifthe concentrations ofstimulus in seawater 6: 27-40.
had varied significantly between studies, then the differ- Derby, C. D., and J. Atema. 1982. The function ofchemo- and me-
chano-receptorsin lobster(Homarusamericanus)feedingbehavior.
ences in threshold response measured in these investiga- J. Exp. Biol. 98:317-327.
tionsmay have been moreapparent than real. Given that Egan, J. P. 1975. Signal Detection TheoryandROCAnalysis. Aca-
marine organisms live in a noisy chemical environment, demic Press, NewYork.
measurements ofthe ability to distinguish between stim- Fuhrman,J.A.,andT.M.Bell. 1985. Biologicalconsiderationsinthe
ulusand background are required. Determinationsofjnd measurementsofdissolved freeamino acids in seawaterand impli-
cationsforchemicaland microbialstudies.Alar. Ecol. Prog.Ser 25:
thresholds, therefore, are critical to an understanding of
13-21.
chemically mediated behavior in the sea. Fuzessery,Z. M.,andJ.J.Childress. 1975. Comparativechemosen-
sitivitytoaminoacidsandtheirroleinthefeedingactivityofbathy-
pelagicand littoralcrustaceans. Biol. Bull. 149: 522-538.
Acknowledgments Garrasi,C.,E.T.Degens,and K. Mopper. 1979. Thefreeaminoacid
The author expresses his gratitude to J. Favuzzi and ctioomnp.oMsairt.ioCnhoefms.ea8w:a7t1e-r85ob.tained withoutdesaltingandconcentra-
Dr. J. J. Childress for providing use ofthe HPLC. This Gleeson, R. A., M. A. Adams, and A. B. Smith, III. 1984. Charac-
research was performed at U. C. Santa Barbara in the terizationofasex pheromone in thebluecrab, Callmectessapidus:
laboratory of Dr. J. F. Case, who graciously gave both crustecdysonestudies.J. Chem. Ecol. 10:913-921.
winatselplreectpuaarledanatdUmnaitveerrisailtysoupfpWoarsth.inTghteonf,inaFlrimdaanyuHsacrrbipotr GHardefePinse,ylcdhD,o.pMhM.y.s,Gi.ca,sn.adnIdJC.riDeA.g.eSrcShwPeeuutbeslri..sh1i19n97g845.C.omSpEiavginndayel.nDcNeeteefwcortYiaoornsko.Tluhbeloerymeatna-d
Laboratories, using computing and library facilities gen- morphic inducer in Phestilla: ecological and biological data. Bull
erously provided by Dr. A. O. D. Willows, Director. Spe- Mar. Sci. 37: 556-566.
426 R. K. ZIMMER-FAUST
Hoel, P. G., S. C. Port, and C. J. Stone. 1971. Probability Theory Raimondi.P.T. 1988. Settlementcuesanddeterminationofthevertical
Houghton Mifflin Company, Boston. limitofan intertidal barnacle. Ecology69:400-407.
Jensen, G. C. 1989. Gregarious settlement by megalopae ofthe por- Rebach, S., D. P. French, F. C. von Staden, M. B. Eilber, and V. E.
celaincrabsPelrolislhescinctipes(Randall)andP. eriomernsStimp- Byrd. 1990. AntennularsensitivityoftherockcrabCancerIrroratus
son.J. Exp. Mar. Biol. Ecol. 131: 223-231. to food substances. / Crust. Biol. 10: 213-217.
Jones, B. N., S. Paabo, and S. Stein. 1981. Amino acid analysisand Sammarco, P. W., J. C. Coll, S. La Barre, and B. Willis. 1983.
enzymatic sequence determination ofpeptides by an improved a- Competitivestrategiesofsoftcorals(Coelenterata: Octocorallia): al-
phthaldialdehyde precolumn labelingprocedure. J. Lig. Chromalogr. lelopathiceffectsonselectedscleractiniancorals.CoralReefs1: 173-
4: 565-586. 178.
Keidel, W. D., U. O. Keidel, and M. E. Wigand. 1961. Adaptation: Schmitt,B.C.,andB.W.Ache. 1979. Olfaction:responsesofadecapod
lossorgainofinformation?Pp. 319-338inSensoryCommunication: crustaceanareenhanced by flicking. Science205: 204-206.
Contributionsto tin'Symposium on Principles ofSensory Commu- Shumake,S. A.,J.C.Smith,andJ.C.Tucker. 1969. Olfactoryinten-
nication. W. A. Rosenblith. ed. M.I.T. Press,Cambridge. sity-difference thresholds in the pigeon. J. Comp. Physiol. Psychol.
Kuris, A. M. 1971. Population interactionsbetween ashorecraband 67: 64-69.
twosymbionts. Ph.D. Dissertation, UniversityofCalifornia,Berkeley. Sih, A., and R. D. Moore. 1990. Interacting effects ofpredator and
La Barre, S.C.,J.C. Coll, and P. W.Sammarco. 1986. Competitive prey behavior in determining diets. Pp. 771-796 in Behavioural
strategiesofsoftcorals(Coelenterata: Octocorallia) III. Spacingand MechanismsofFoodSelection. R. N. Hughes, ed. Springer-Verlag,
aggressiveinteractionsbetween alcyonaceans. Mar. Ecol. Prog. Ser. London.
28: 147-156. Slotnick, B. M., and J. E. Ptak. 1977. Olfactory intensity-difference
Laverack, M.S. 1988. Thediversity ofchemoreceptors. Pp. 287-312 thresholdsin ratsand humans. Physiol. Behav. 19: 795-802.
inSensoryBiologyofAquaticAnimals. J. Atema, R. R. Fay, A. N. Snow, P.J. 1973. Theantennularactivitiesofthehermitcrab,Pagurus
Popper,and W. N. Tavolga,eds. Springer-Verlag, NewYork. alaskensis(Benedict). / Exp. Biol 58: 745-765.
Lindberg, R.G. 1955. Growth,populationdynamicsandfieldbehavior Sweatman, H. 1988. Field evidence that settlingcoral reeffish larvae
ofthespinylobster,Pamilirusnnerruptus(Randall). L'niv. Cal.Publ. detect resident fishes using dissolved chemical cues. / Exp Mar.
Zoo/. 59: 157-248. Biol Ecol. 124: 163-174.
Lindstedt, K. J. 1971. Chemical control offeeding behavior. Comp. Trapido-Rosenthal,H.G.,R.A.Gleeson,and W.E.S.Carr. 1990. The
Biochem. Physiol. 39A: 553-581. efflux ofamino acids from the olfactory organ ofthe spiny lobster:
Manahan,D.T.,S.H.Wright,andG.C.Stephens. 1983. Simultaneous biochemicalmeasurementsandphysiologicaleffects. Biol. Bull. 179:
determinationsofnetuptakeof16aminoacidsbyamarinebivalve. 374-382.
Am. J Physiol. 244: R832-R838. Yancey,P.H.,M.E.Clark,S.C.Hand,B.D.Bowlus,andG.N.Somero.
McBurney,D.H.,R.A.Kasschau,and I,.M.Bogart. 1967. Theeffect 1982. Livingwithwaterstress:evolutionofosmolytesystems.Sci-
ofadaptation on tastejniis. Percep. Psychophys. 2: 175-178. ence111: 1214-1222.
Miller, R. L. 1989. Evidence for the presence ofsexual pheromones Zimmer-Faust, R. K. 1987. Crustacean chemical perception: towards
in free-spawningstarfish. J. Exp. Mar Bio/. Ecol. 130: 205-221. atheoryonoptimalchemoreception. Biol. Bull. 172: 10-29.
Moore, P., and J. Atema. 1988. A model ofa temporal filterin che- Zimmer-Faust,R. K. 1989. Therelationshipbetweenchemoreception
moreceptiontoextractdirectional information fromaturbulentodor and foragingbehaviorin crustaceans. Limnol. Oceanogr. 34: 1364-
plume. Biol. Bull 174: 355-363. 1374.
Mopper, K.,and P. Lindroth. 1982. Diel and depth variationsindis- Zimmer-Faust, R.K.,andJ.F.Case. 1982. Organizationoffoodsearch
solvedfreeaminoacidsandammoniumintheBalticSeadetermined inthekelpcrab,Pugetliaproducta(Randall).J. Exp. Mar.Biol.Ecol.
by shipboard HPLCanalysis. Limnol. Oceanogr 27: 336-347. 57: 237-255.
Morse, D. E. 1990. Recent progress in larval settlement and meta- Zimmer-Faust, R. K., and E. Spanier. 1987. Gregariousness and so-
morphosis:closingthegapsbetween molecularbiologyandecology. cialityinspinylobsters:implicationsfordenhabitation./ Exp.Mar.
Bull Mar. Sci. 46:465-483. Biol. Ecol 105: 57-71.
Pearson, W. H., and B. L. Olla. 1977. Chemoreception in the blue Zimmer-Faust, R. K., J. M. Stanfill, and S. B. Collard, III. 1988. A
crab(Callmcctcssapulus). Biol Bull 152: 46-54. fast, multichannel fluorometer for investigating aquatic chemore-
Pearson, W. H., P. C. Sugarman, D. L. Woodruff, and B. L. Olla. ception andodortrails. Limnol. Oceanogr. 33: 1586-1595.
1979. ThresholdsfordetectionandfeedingbehaviorintheDunge- Zimmer-Faust, R. K., J. E.Tyre, and J. F. Case. 1985. Chemical at-
nesscrab. Cancermagister(Dana). J E\p. Mar. Biol. Ecol. 39:65- tractioncausingaggregationinthespinylobster,Panulirusinterniptus
78. (Randall), and its probable ecological significance. Biol. Bull 169:
Peckarsky, B. L. 1980. Predator-prey interactions between stoneflies 106-118.
and mayflies: behavioral observations. Ecology61: 932-943. Zimmer-Faust, R. K.,J. E.Tyre, W. C. Michel, and J. F. Case. 1984.
Pfaffman, C, L. M. Bartoshuk, and D. H. McBurney. 1971. Taste Chemical mediation ofappetitivefeedinginamarinedecapodcrus-
psychophysics. Pp. 75-101 inHandbookojSensoryPerception. \'ol. tacean: theimportanceofsuppressionandsynergism. Biol. Bull 167:
/I'. L. M. Beidler, ed. Springer-Verlag, New York. 339-353.
Price, R. B., and B. W. Ache. 1977. Peripheral modification ofche- Zurburg, \\., and A. DeZwaan. 1981. The roleofaminoacidsin an-
mosensoryinformation inthespinylobster. Comp. Biochem Physio/. aerobiosisand osmoregulation in bivalves. / Exp. Zool. 215: 315-
57A: 249-253. 325.