Visual Rhythms in Stomatopod Crustaceans Observed in the Pseudopupil

10 Pages·1992·4.5 MB·English

by  T W Cronin

Reference: Biol. Bull 182: 278-287. (April, 1992)
Visual Rhythms in Stomatopod Crustaceans Observed
in the Pseudopupil
THOMAS W. CRONIN
Department ofBiological Sciences, University ofMaryland Baltimore County,
Baltimore. Maryland 21228
Abstract. Many aspects of visual function in animals terns also express rhythmicity in membrane shedding
are influenced by the operation ofendogenous rhythms. (Nassel and Waterman, 1979; Horridge et al. 1981; Wil-
Usingtechniques ofintracellular optical physiology, I in- liams, 1982) or preparation for shedding (Chamberlain
vestigated visual rhythms in two species of stomatopod and Barlow, 1984). Visual rhythms apparently unique to
ERG
crustaceans (mantis shrimps): Sqiiilla empusa. a species invertebrates include cyclic changes in amplitude
active throughout the day and night, and Gonodactylm (e.g., Arechiga and Wiersma, 1969; Page and Larimer,
oerstedii, which isstrictlydiurnal. Reflectance from within 1975; Barlow, 1983;FleissnerandFleissner, 1985),inrates
thedeeppseudopupil ofthecompoundeyesanditschange ofaction potential production (Jacklet, 1969), and, par-
upon stimulation with lightwere monitored in individual ticularly in arthropods, migration of screening pigment
animals in constant conditions foruptotwoweeks. Both in secondary pigment cells(Welsh, 1930; Kleinholz, 1937;
species expressed circadian rhythms in visual function. Page and Larimer, 1975; see reviews ofStavenga, 1979,
In S. empusa, the pupillary response was much stronger and Autrum, 1981).
duringsubjective night; littleornoresponsecould beelic- In many cases, circadian changes in sensitivity aredue
itedduringsubjective day. In thisspecies, an endogenous primarily to variations in the quantum catch by the pho-
rhythm caused pupillary reflectance to increase during toreceptor cells, produced by alterations either in asso-
subjective day. Rhythms in G. oerstedii were of lower ciated structures such as secondary pigment cells or in
amplitude than in S. empusa and were more difficult to the amount ofphotoreceptor membrane per cell. But in
detect. Thedifferencesbetweenthesespecies,togetherwith some species, the actual photoreceptor cells can undergo
the results of other comparative research on visual rhythmic changes that affect their ability to respond to
rhythms in arthropods, suggest that circadian, rhythmic the capture of a photon by rhodopsin. For example, in
processes are involved in optimizing nocturnal eyes for Limuluspolyphemus. circadian events alter electrophys-
maximum sensitivity and dynamic range. iological properties of individual photoreceptor cells
(Kaplan and Barlow, 1980; Barlow etal., 1987; Kassand
Introduction Renninger, 1988).
Endogenous rhythms in visual function are common The photoreceptorcells ofmany arthropod species are
independentlycapableofadjustingtheirsensitivitytolight
amonganimals. Diverse rhythmicphenomenaassociated
by mobilizing granules ofprimary pigment, producing a
with vision occurin both vertebrateand invertebratespe- phenomenon known asthe pupillary response(Kirschfeld
cies. Forexample, in the vertebrates, events known to be and Franceschini, 1969; see review of Stavenga, 1979).
under endogenous control include photoreceptor mem- Arthropod pupillary responses may be observed nonin-
brane shedding (LaVail, 1976), retinomotor movements vasivelyby monitoringlight reflected fromthedeeppseu-
(reviewed in Levinson and BurnsmidRe,NA1981; Burnside and dopupilofthecompoundeye(Stavengaand Kuiper, 1977;
Nagle, 1983), and synthesis of coding for opsin Bernard and Stavenga, 1979; Cronin, 1989); as the pig-
(Korenbrot and Fernald, 1989i Invertebrate visual sys- ment granules migrate inwards in response to photic
stimulation, reflectance rises. Circadian changes in pseu-
Received24October 1991; accepted 13January 1992. dopupillaryappearanceandlevelofreflectancehavebeen
278
STOMATOPOD VISUAL RHYTHMS 279
observed in many arthropod compound eyes (Stavenga, ofthe eye (see photographs in Cronin, 1986, and Cronin,
1977; see review ofStavenga, 1979). The rhythmsare ap- 1989)wascenteredwithin the fieldofviewofan incident-
parently due to circadian events in secondary pigment light, photometric microscope. The entire apparatus was
cells, under nervous (Page and Larimer, 1975) or neu- housed in a dark box with a black curtain covering the
roendocrine (Smith, 1948; Page and Larimer, 1975; Her- front, and experiments took place in a room that was
nandez-Falcon et ai, 1987) control. True pupillary re- completely blacked out and isolated from external sources
sponses, however, are caused by translocations ofprimary oflight.Thecentral regionofthepseudopupil understudy,
pigments, within the actual photoreceptor cells, in direct which appeared to glow dully when viewed by eye, was
responsetophoticstimulation (Stavenga, 1979). Dothese isolated using an adjustable field diaphragm. Reflectance
responses also express circadian rhythms? Ifso, the eyes from the pseudopupil was monitored as described in
may be optimized for sensitivity and dynamic range at a Cronin (1989), using light of wavelengths >720 nm
particularphaseofthedielcycle, underrhythmiccontrol. (Schott RG720 longpass filter, usedwithSquilla) or>800
In earlier work with the squilloid stomatopod crusta- nm (Schott RG800 longpass filter, used with Gonodac-
cean Squilla empitsa, I found that it was difficult or im- tylus); thissource oflight illuminated the eye continually
possible to elicit any changes in reflection from the deep throughout each experiment, and by itself caused no
pseudopupil during the day, whereas nocturnal stimula- measurable pupillary response. At20-or30-min intervals,
tionproduced large, highlyrepeatablereflectanceincreases a stimulating exposure automatically was provided, pro-
(Cronin, 1989). Incontrast, thegonodactyloidstomatopod duced by passing light from a 150-W Xenon arc through
species Gonodactylus oerstedii and Pseitdosquilla ciliata a monochromator (Oriel 7250 with 500-nm blazed grat-
expressed pupillary responses no matter when they were ing), counter-rotating 10-cm diameter neutral density
stimulated. In this report, I describe experiments testing wedges, and a linear polarizing filter. All stimuli were
whetherthereisarhythmiccomponent to pupillary func- confined to the ommatidia contributing to the pseudo-
tion in S. empusa and G. oerstedii. The results suggest pupil under study, and were at a wavelength of500 nm
that rhythmic events strongly alterthe pupillary responses (halfbandwidth of 10 nm). Theywereproduced byopen-
ofS. empusa and have a weaker influence on those ofG. ing a Uniblitz electromagnetic shutter under the control
oerstedii. ofamicrocomputer, and lastedfor5 min(Squillaempusa)
or 30 s (Gonodactylus oerstedii). Measurements of light
Materials and Methods reflected from the pseudopupil commenced before each
exposure and continued until well afterwards, and data
Adultanimalswereused inallexperiments. Workwith were stored on the microcomputer's hard disk for later
Squilla empusa was carried out at the Duke University analysis. The response for each stimulus was defined as
Marine Laboratory in Beaufort, NorthCarolina. Animals the average reflectance during the final 20% ofthe stim-
were collected locally and maintained either in running ulation's duration, divided by the average reflectance be-
seawater tables exposed to indirect, natural daylight fore stimulus onset and following a period in the dark
through windows along two sides ofthe room (ambient equal totheduration ofthestimulusitself(seealsoCronin
photoperiod experiments) orin small containerscontain- and King, 1989). Responses are plotted asthe percentage
ingnatural seawaterplaced in achamberwith acontrolled change in reflectance relative to the average dark levels.
light:dark cycle (reversed photoperiod experiments). An- In some cases, the sensitivity ofthe pupillary response
imals were fed fresh oysterand shrimp meat. Experiments was measured by providing a series ofstimulating inten-
with Gonodactylusoerstediitook placein Baltimore, using sities over a range of 3.5 to 3.8 density units at steps of
animalscollected in the Florida Keys. Theseanimalswere 0.5 units. Each serieswas produced under microcomputer
kept in aquaria filled with artificial seawater in a 12 h:12 control, by rotatingthe neutral density wedges to a series
h light:dark cycle, and were fed frozen shrimp. of preprogrammed settings. The intensity ofthe stimu-
Reflectance from thedeeppseudopupil was monitored lating source was measured for each experiment using a
using the techniques of intracellular optical physiology, calibrated PIN-10DP/SB photodiode (United Detector
described in detail in Bernard and Stavenga (1979) and Technology) placed at the position ofthe animal's eye.
Cronin (1989). Dorsal surfaces ofanimalswere attached,
usingScutan dental plastic, toa moveable platform which Results
wasthen submersed in seawater. Duringeach experiment,
water in the experimental chamber (which contained Earlierwork with Squilla empusa hadrevealedthatthe
about 1200 ml) was changed occasionally, at irregular ability ofan animal to express pupillary responsesappar-
times. Animals were not fed during an experiment. entlyvariedwith time. Resultsofanexperimentdesigned
Once mounted, each experimental animal wasaligned to detect rhythms in responsiveness are shown in Figure
sothatthe pseudopupil ofeitherthedorsal or ventral half 1. The animal, a male of body length (rostrum-telson)
280 T. W. CRONIN
Concurrently, baseline pseudopupillary reflectance de-
creased by up to 50%. Near the time ofsubjective dawn,
thechange in reflectanceduringstimulationdropped once
more to near zero, again over a period of 1 to 2 h, while
the baseline reflectance quickly rose to its daytime level.
This rhythmical pattern was typical ofthat expressed in
animalsmaintained undertheambient photoperiod. The
period ofthe rhythm was estimated using Enright's per-
iodogram technique (Enright, 1965); both rhythms had
periods near 24 h (see Fig. 1; the difference between the
twoperiodsismeaninglesswithtimeseriesofthislength).
It is conceivable that the observed rhythms in baseline
reflectance and responsivenesswereexpressionsofasingle
phenomenon; the pupillary mechanism could rhythmi-
cally assume its fully light-adapted state during the day,
thus increasing reflectance and losing its ability to adapt
further to light. Two types ofobservations argue against
this interpretation ofthe data. First, the two rhythms did
not haveexactlyinverse forms. Baselinereflectancetended
tochange lessabruptlythan didthe level ofresponse, and
on somedaysitschangeswere notprecisely in phasewith
Day the changes in response level. More convincingly, some
Figure 1. Lightreflectancefromthedeeppseudopupil(Reflectance; animals expressed rhythms in responsiveness with little
top panel)and percentage change in reflectance on stimulation (% Re- or no circadian change in the baseline reflectance. For
sponse; bottom panel) in an adult male individual ofSquilla empusa example, in the experiment of Figure 2, the baseline re-
maintainedinconstantconditions.Measurementsweremadeat30-min
intervals for a total of327 intervals, from 7 to 14 July 1987. Stimuli
were at 500 nm, at a quantal intensity of2.9 X 10" quanta cm"2 s~'.
The reflectancewasmeasured asdescribed in thetext for 1 min before 100
each5-minstimulation;averagevaluesareplottedonascalenormalized .Vn) 80
tothelargestvalueobtained. Percentresponsewascalculatedasdescribed o C
in the text. Vertical lines are drawn at successive midnights. The light
and dark bands on the abscissa represent times ofnatural sunrise and
sunset(Eastern DaylightTime). Theperiod(T)ofeach rhythm, in h, is
giveninthetoprightcornerofitspanel. Eachtimeserieswasanalyzed
using Enright's periodogram technique (Enright, 1965). Penodogram
amplitudes were computed at 0.1-h intervals for periods from 10 h to
30 h. The value given on the graph is that ofthe period in this 20-h
range havingthegreatest amplitude.
85 mm,was placed in constant darkness in the apparatus
at midday on the first day and stimulated each 30 min
for the next 7 days.
The results ofthe experiment ofFigure 1 aretypical of
those of most experiments. Rhythmical variations oc-
curred both in the level ofthe pupillary response and in
the reflectance from the pseudopupil in the absence of
stimulation. During the subjective day, pseudopupillary
reflectance remained high, and little or no measurable
reflectance change occurred in response to the light stim-
ulus the variations that were observed were due to ap-
parently random fluctuations. However, nearthe time of
natural sunset, reflectance from the deep pseudopupil di-
minished, andlargeincreasesin reflectanceoccurred upon
stimulation. Within 1 io 2 h, the reflectance rise during
stimulation changed from near zero to greaterthan 20%.
STOMATOPOD VISUAL RHYTHMS 281
flectance varied only slightly over four days. The only The rhythms of responsiveness in these experiments
changeswere a small increase during first dark phase and retained phases that appeared to be tightly linked to the
transient changes on each successive dusk and dawn. externaldiel cycle, andthereremained thepossibilitythat
These results strongly suggest that the ability ofthe pu- external timing cues were reaching the experimental an-
pillary mechanism itselfto respond to light varies rhyth- imals. This possibility was tested by placing an animal in
mically. Changes in baseline reflectance could not result anisolatedchambersubjectedtoalight:darkcyclephased
fromarhythmical responsivenesstotheconstant 720-nm differently from the ambient cycle ofsunrise and sunset;
lightusedtomonitorreflectance, forsucharhythmshould lights were switched on at 1800 (Eastern Daylight Time)
produce increasing pseudopupillary reflectance at night, and offat 0600 each day. Following 12 days ofexposure
when responsiveness isgreatest. I therefore conclude that to this "inverted" photoperiod, an animal was placed in
although the two rhythms observed in Figure 1 may be constant conditions. Rhythms both of the pupillary re-
intimately linked, they are expressions ofseparate events sponse and the baseline reflectance were now observed to
within the ommatidia. Once again, periodogram analysis be in phase with the imposed cycle. Responsiveness in-
suggests that the rhythms ofFigure 2 are circadian. Per- creased, and baseline reflectance decreased, during the
iodogram analysisisparticularlyunreliablefortimeseries entrained dark period between 6 am and 6 pm. To avoid
as short as that ofFigure 2, but inspection ofthe forms repeatedly stressing the animal by mounting it for study,
oftherhythmsclearlyconfirmsthattheirperiodsare near itsvisual rhythmswere notexperimentallydefined before
24 h. imposingthe reversed photoperiod. Nevertheless, thiswas
The onset ofresponsivenessatdusk occursbyasmooth the only case in which maximum responses were ever
transition(Fig. 3). Although successive responsesincrease observed during the astronomical day, so it is reasonable
in size, the time each takes to reach its plateau phase is to conclude that the rhythms had been entrained by the
similar. It is not primarily the rate ofthe response that exposureto the"inverted" photoperiod. Such resultsalso
alters,therefore,buttheactualamplitudeofthereflectance demonstrate that the rhythms observed in the earlier ex-
change. The increasing sizes ofthe responses during the periments were not in response to exogenous cues. As
dusktransition mimictheincreasingresponsesthat occur before, the periods ofthe rhythms were very near 24 h
with increasing intensity, when theeye is maximally sen- (Fig. 4).
sitive (Cronin, 1989). The dusk transition, therefore, ap- Response-mros-intensity functions were obtained
pears to be a time ofrapidly increasing sensitivity ofthe from the individuals studied in Figures 2 and 4 during
pupillary mechanism. both the subjective night and the subjective day. The
o
Q.
u
Oi
figure 3. Changes in reflectance from the deep pseudopupil ofthe animal used in the experiment of
Figure 2. during the onset ofthe nocturnal increase in responsiveness. The 6 traces were obtained at 30-
min intervals, beginning at 1535 EOT (lowest trace) and ending at 1805 (highest trace) on 19 July 1987.
Percent response iscomputed relativetotheaverage reflectanceinthe 1 minpriortostimulation. Vertical
linesaredrawn atthe beginning(0 min)andend (5 min) ofthe stimulation interval.
282 T. W. CRONIN
100
Day
Figure4. Resultsobtained froma femaleSquilla empusamaintainedinconstantconditionsfrom I to
1 1 July 1988. Priorto theexperiment, the animal was kept in a controlled light:dark cycle asdescribed in
thetext;thelightanddark bandsontheabscissaindicatethetimesoflightanddarkoftheentrainingcycle.
Arrowsindicate timesofthe beginningsofseriesduring which stimulation wasincreased duringeach half
hour. Atall othertimes, stimulationwasataquantal intensity of 1.02 X 10" quantacnT:s~'.Gapsin the
record indicatetimesofmissingdatadue toequipment failure;otherwiseasin Figure 1.
functions were obtained by stimulating the eye on 8 or(| ticular diel variation in the pupillary responses was no-
successive 30-min intervalswith stimuli increasingatstep; ticed. Nevertheless, it seemed likely that gonodactyloids
of0.5 logunits, ultimatelyprovidingamaximum quantal could possess rhythmssimilartothose ofSquilla, butper-
intensity of 3.44 X 10'2 quanta cirT2 s~' (experiment of haps more subtlein theirform. Thispossibilitywastested
Fig. 2) or 2.62 X 1013 quanta cm"2 s"' (experiment of with Gonodactylusoerstedii, usinganoverallexperimental
Fig. 4). design like that employed with Squilla empusa, except
All nighttime series produced response-vm;-intensity that in these cases entrainment was imposed entirely by
functions ofsimilar shape, with maximal reflectance in- artificial cycles oflight and dark. The pupillary response
creases near 13% (Fig. 5A) or45% (Fig. 5B). In contrast, is much more rapid in G. oerstedii than in S. empusa, so
thedaytime response level remained near0, risingat most I used briefer, more frequent stimuli in these experiments.
to about 3% of the height of the nighttime peak at the Resultsoftwoexperiments, representing the range ofob-
maximum stimulation intensity. It appears, in fact, that served experimental outcomes, are displayed in Figures
the maximum pupillary response that can be generated 6 and 7.
is greatly reduced during the day. To test this conjecture In the experiment of Figure 6, reflectance from the
would require stimuli far more intense than what was pseudopupil priortostimulation showedaclearcircadian
available in these experiments. The highest intensities to rhythm. Here, the form was rather different from what
which the animal was exposed during these series were was obtained using S. empusa. Soon after the expected
up to 100 times the usual test exposure; somewhat sur- time oflights-out, reflectance from the deep pseudopupil
prisingly, these produced no obvious phase shifts in sub- slowly increased, ultimately becomingabout 10% greater
sequent cycles ofthe rhythms (Figs. 2 and 4). than during the subjective day. Beginning near midday
In the earlier work with gonodactyloid stomatopod in the entrainment cycle, this elevated reflectance once
species (Cronin, 1989; Cronin and King, 1989), no par- moredeclined. A rhythm in pupillary responsivenesswas
STOMATOPOD VISUAL RHYTHMS 283
12
10
o
D.
-3 -2
Log Intensity
Figure 5. Response-vtTOu-intensity functions obtained during the experiments ofFigure 2 (A) and
Figure4(B).Functionswereobtainedatthetimesindicatedbyarrowsonthosefigures;largecirclesindicate
resultsobtainedduringsubjectivenightandsmallcircles,duringsubjectiveday.Opencirclescorrespondto
thefirstseriesandclosedcirclestothesecond. Photicintensitiesarerelativeto3.44 x 1012quantacm"2s~'
more difficult to detect, although on average, responses were more difficult to detect than in S. empusa, but they
did appear to be slightly larger at subjective night. Per- could be observed in some individuals.
iodogram analysis of the data suggests the presence of The rhythms that were observed were robust. They
circadian cycles in both the baseline reflectance data and persisted and maintained their form, frequently with a
the responsiveness data (Fig. 6). highamplitude, foraweekormoreinconstantconditions.
The experiment of Figure 7 revealed the strongest The rhythms were clearly circadian; their periods were
expression ofcircadian rhythms in responsiveness that I consistently revealed to be near 24 h eitherby inspection
observed in over 20 experiments with G. om/tW//. Am- or by periodogram analysis ofthe data. The rhythm in
plitudesofthepupillary responsewereabouttwiceaslarge responsiveness expressed by S. empusa was particularly
during subjective day as during subjective night, thus impressive for its rapid rise each subjective evening and
havingthe opposite form ofthoseexpressedby5. empma. its equally rapid fall in the morning.
The pupillary response was present both during the day Duringtheday,thesensitivityofthepupillaryresponse
and night. In this case, however, there was no evidence decreased by at least three orders of magnitude. These
ofa circadian cycle in pupillary reflectance. changesaregreaterthan observed inLimuluspolyphemus.
in which both the electroretinogram (ERG) and single-
Discussion
cell sensitivities decrease by about 1.5 log units (Barlow
Asdemonstrated here, rhythmswithacircadian period et al., 1977, 1987). Otherarthropods, however, have sen-
can readily be observed through observations of pseu- sitivity changes between the day and night states about
dopupils in compound eyes ofstomatopod crustaceans. as large as those of S. empusa. In the crayfish Cherax
In the squilloid species, Squilla empusa. two parallel destructor, dark-adapted single photoreceptor cells are
rhythms ofhigh amplitude are usually observed: a cycle morethan two logunits more sensitiveat night(Bryceson,
inbaselinereflectancefromthepseudopupilintheabsence 1986), while the simple eyes of scorpions rhythmically
of stimulation, and a cycle in the amplitude ofthe pu- gain nearlyfourlogunitsofsensitivityeach night(review:
pillary responsetolight stimulation. In someexperiments, Fleissner and Fleissner, 1985). In its natural habitat, 5.
the gonodactyloid Gonodactylus oerstedii expressed the empusa probably lacks a pupillary response during the
baseline reflectance rhythm, although at loweramplitude day. The maximum intensities of stimulation used in
than5. empusa. Rhythmsinresponsivenessin G. oerstedii producing the response-irrws-intensity functions ofFig-
284 T. W. CRONIN
_ 100 and Larimer, 1976), and no other extraretinal photore-
ceptors have yet been described in stomatopods. If en-
trainment is mediated solely by the compound eyes, the
spatially limitedstimuli oftheseexperiments(whichwere
restricted to the ommatidia of the pseudopupil of one
part ofasingle eye) must havebeen insufficientto induce
observable phase changes. Nevertheless, intense stimuli
like those used to measure the response-vmzw-intensity
functions produce no obvious phase shifts, implyingthat
there may be a role for extraocular photoreception in
rhythm entrainment in stomatopods.
What underlying events take place within the com-
pound eyes to bring about the rhythms observed in this
study? Changes in the level ofbaseline reflectance can be
effected in several ways (Stavenga, 1979). External to the
receptor cells, these include reorganization of optical
structures or associated pigment cells, movement ofpig-
ment in secondary pigment cells, and masking or un-
maskingofatapetum. Withinthephotoreceptors, changes
in reflectance could be caused by alterations in rhabdom
size or microvillar organization, or by events within the
Figure 6. Results obtained from a female Gonodactylus oerstedii
maintained in constant conditions from 22 to 28 January 1988. The 100
animal was kept in a controlled light:dark cycle, indicated by the light
and dark bands on the abscissa, prior to the experiment. Stimulation
wasat500nm,atintervalsof20min,andataquantalintensityof1.57
X 1012quantacm'2s~'. Otherwiseasin Figure 1.
ure 4, on the order of 10" quanta cm 2 s ', are similar
to intensities an animal would experience at a depth of
onlyafewmetersinthecoastalwatersit inhabits(Forward
el al.. 1988). During the daylight phase ofthe rhythm,
such intensities produced no apparent response.
Ifthese circadian rhythmsare to be properly phased to
the diel cycle, they must be entrainable by cycles oflight
and dark. Animals apparently do entrain completely to
a novel light:dark cycle within 12 days, as suggested by
the results of the experiment of Figure 4. Presumably,
photoreceptors for this entrainment are either within the
compound eyes or exist elsewhere in the animal. In fact,
many invertebrate species entrain theircircadian rhythms
usingextraocularpathways(see reviewofBennett, 1979).
In crayfish, and probably other decapod crustaceans,
photicentrainmentofcircadian rhythmscan beachieved
by retinal illumination (Larimer and Smith, 1980), but maiFnitgauirneed7.incRoenssutlatnstcoobntdaiitnieodnsffrroomma31mJaalneuarGyontooda1c2tFyelbursuaoreyrs1t9e9d1i.i
suchentrainment mayalso involve photoreceptorsofthe The animal was kept in a controlled lightidark cycle, indicated by the
6th abdominal ganglion (Fuentes-Pardo and Inclan-Ru- lightanddarkbandsontheabscissa,priortotheexperiment.Datafrom
bio, 1987)orotherregionsoftheCNS(Pageand Larimer, the first two days ofthe experiment are not plotted, due to repeated
op1fh9o7Pt6ao;greLeacaernpidtmoeLrrasrai(nmidnertShm(ei1t96h7t,6h)1ad9be8md0)oo.nmsiItnnraaplatregtdainctughllaaitro,nt)htehaecraewuodnraoklt aacrtenmfii~lmne2atcelstr"avnm1a.colePsv)eeorpfmiroe2od0ndoutmgcireanadn,mdaaaennsqaldluoyiwastlpiymsaeroqnifustaitnnhfgteaiapdllueartniean.otdoeSofntsgitirmhteuaylmuoapftwpii1eot.rnh97pwaaaxnssepl1ia0tk(e|p:5up0qpe0iualalnknamtra.ayt
required for entrainment. In contrast to decapod crusta- 27.1 h;because the analysisproduced noclearmaximum, the valueot
ceans, S. empusalacksthiscaudal photoreceptor(Wilkens r isnotgiven on the figure. Otherwiseasin Figure 1.
STOMATOPOD VISUAL RHYTHMS 285
cytoplasm ofretinularcells, such as rearrangement ofthe concentration (see review ofFein and Payne, 1989), the
perirhabdomal palisade or movements ofpigment gran- absence of the pupillary response during the day could
ules. imply that electrophysiological responses of the photo-
Ommatidial reorganization no doubt accounts for receptorsare also abolished at that time. However, this is
much ofthe circadian change in the appearance of the unlikelytobethecase; Kirschfeldand Vogt(1980)showed
pseudopupil ofLimuluspolyphemus(Slavenga, 1979), but that in fly photoreceptors, it is possible to block pigment
more recent work suggests that the retinularcell pigment migration without changing retinal electrical responses.
itselfmigrates under circadian control (Kier and Cham- In work with mutant flies, Lo and Pak (1981) also ob-
berlain. 1990). Long-term studies ofanatomical changes served that electrophysiological responses could remain
in stomatopod eyes do not exist. In work with the Med- in the absence of pigment migration. The processes of
iterranean species Squilla mantis, SchifF(1974) stated that pigment translocation and membrane depolarization,
duringdark adaptation, rhabdoms increase in length and while both calcium-dependent, are therefore not com-
decreaseindiameter; simultaneously, thecrystallinecone pletely parallel. The diurnal loss ofpupillary responsive-
contracts. Schonenberger (1977) also observed the con- ness in Squilla empusa could represent another example
traction of the crystalline cone during dark adaptation, ofthedecouplingofthesetwoprocesses. Experimentsare
and noted that the distal pigment cells reorganize at that desirable in which the electrical and pupillary responses
time. Within the photoreceptorcells, granulesofprimary are monitored simultaneously in this species.
pigment line up in neat rows, encircling the rhabdom as Despite having radically different anatomies, the com-
it dark adapts. These changes occur during diurnal dark pound eyes ofS. empusa and Limulus polyphemus are,
adaptation, following prolonged exposure to daylight, at to some extent, analogous in the functioning oftheir pu-
times when Squilla empusa reveals no light-sensitive pu- pillary responses. Both express rhythmic changes in re-
pillary responses and no evidence ofdark adaptation fol- flectance from the deep pseudopupil, and both show
lowing stimulation. At present, it is uncertain whether changes in this reflectance only at night (see Stavenga,
thesetwospeciesofSquilladifferintheirabilitytorespond 1979). Interestingly, demands on their visual systems
to light during the day, whether the two sets of studies throughoutthecourseofeachday mayalsobeanalogous.
involve different phenomena, or whether prolonged ex- Neither species is entirely inactive during the day, but
posure to light during the day can in fact produce revers- mating ofLimulus, a behavior involving vision (Barlow
ible light-adaptation via the pupillary mechanism. et al., 1982), occurs mostly during twilight or night (Bar-
While cyclic restructuring ofommatidia or transloca- low et al., 1986). Indeed, nocturnal vision in Limulus is
tion of secondary pigment could produce rhythmic extraordinary, enablingthedetectionofhigh-contrasttar-
changes in baseline reflectance, events effecting majoral- gets under starlight (Barlow et al., 1982). Activity cycles
terationsin the level ofthepupillary response must occur ofSquilla empusa have yet to be examined in the field,
within the actual photoreceptor cells. In apposition eyes but in the laboratory, at least, this species is most active
like those ofstomatopods, the pupillary response is pro- during the night (pers. obs.), and the congener, Squilla
duced by radial translocation ofgranules ofprimary pig- mantis, isclearly nocturnal (Frogliaand Giannini, 1989).
ment residingin the photoreceptors(Stavenga. 1979; King The ocular design of 5. empusa is that of a nocturnal
andCronin, 1989). Reflectance changes may be produced animal (Cronin, 1986). It is plausible that the rhythms in
in superposition compound eyes, however, by events in visual function described in this paper are characteristic
secondarypigmentcells(Bernard elal., 1984;Weyrauther, physiological propertiesofa nocturnal compound eye. In
1986). Compared to the responses in stomatopod eyes, fact,throughout thearthropods, regardlessofeyetype, all
these changes are slow and have considerable inertia high-amplitude rhythms in visual physiological function
the process continues, or remains saturated, long after yet described are in nocturnal species. Besides Limulus,
stimulation ceases. these include scorpions(simpleeyes, rhythm in ERG am-
Migration of primary pigment is directly under the plitudeandsensitivity: reviewed in FleissnerandFleissner,
control ofthe retinular cell, and, at least in crustaceans, 1985), crayfish (superposition compound eye, rhythm in
isthought not to be influenced by hormones (Ludolph et ERG amplitude and sensitivity: Arechiga and Wiersma,
al., 1973). In another arthropod, Limulus polyphemus, 1969; Page and Larimer, 1975; Bryceson, 1986), and
ERG
rhythmic neural input does influence the position ofpri- cockroach (apposition compound eye, rhythm in
mary pigment (Kier and Chamberlain, 1990); similar amplitude: Wills et al., 1986).
processes may act in crustacean eyes. The pupillary re- G. oerstedii, unlikeS. empusa. isactiveonly from dawn
sponse requires the presence ofcalcium ions (Kirschfeld to dusk (Dominguez and Reaka, 1988). At evening twi-
and Vogt, 1980; Frixione and Arechiga, 1981; Howard, light, it seals offthe entrance to its burrow and remains
1984). Since excitation ofarthropod photoreceptor cells enclosed all night. Its eyes are optimized for photopic
is also dependent upon intracellular increases in calcium function; indeed, the specialized spectral receptor classes
286 T. W. CRONIN
in itseyes require reasonably bright light to operate at all Cronin, T. W. 1986. Optical design and evolutionary adaptation in
(Cronin and Marshall, 1989; see also Marshall et ai, crustacean compoundeyes.J. Crust. Biol. 6: 1-23.
1991). Because the eye is used primarily for vision when Crontihne,sTt.udWy.of19s8t9o.matAopppoldiccartuisotnacoefaninvtirsaicoenl.luJl.arCoopmtpi.calPhtyesciohln.iqAue1s64t:o
photon capture is not limiting, strong rhythmic cycles in 737-750.
visual function may be unnecessary. Cronin, T. W., and C. A. King. 1989. Spectral sensitivity ofvision in
The expression of high-amplitude circadian visual the mantis shrimp, Gonodactylus oerstedii, determined using non-
rhythms in a primarily nocturnal species like S. empusa, invasiveopticaltechniques. Biol Bull 176: 308-316.
and theirabsence in thediurnal G. oerstedii, couldthere- Cronin, T. W., and N.J. Marshall. 1989. Multiplespectral classesof
fore reveal fundamental differences in function between photoreceptorsin retinasofgonodactyloid stomatopodcrustaceans.
J. Comp. Physiol A 166: 261-275.
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versus diurnal function. If so, the rhythms observed in reef-dwellingstomatopods: a test ofalternative hypotheses. / Exp.
thisstudybymonitoringlightreflectance fromdeeppseu- Mar. Biol. Ecol. 117: 47-69.
dopupilsareamanifestation ofmorepervasive underlying Enright, J. T. 1965. The search for rhythmicity in biological time-
alterations that must occur to maintain visual function series.J. Theoret. Biol. 8:426-468.
atdayand night. The study ofrhythmic cyclesofsensory Feinp,hoAt.o,raencedptRo.rsP:ayrnoele.s1o9f8c9a.lciPuhmoatnodtriannossdituocltitroinspihnosLpihmautel.usPpv.en1t7r1a-l
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Acknowledgments Fleissner,G.,andG.Fleissner. 1985. Neurobiologyofacircadianclock
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This material is based on work supported by the Na- Arachnids, F.G. Barth,ed. Springer, Berlin, Heidelberg. New York.
tional Science Foundation under Grants No. BNS- Forward, R. B., Jr., T. W. Cronin, and J. K. Douglass. 1988. The
8518769 and BNS-8917183.1 thank D. G. Stavenga and visual pigments ofcrabs. II. Environmental adaptations. / Comp.
L. Kass for their comments on an earlier version ofthe Physiol. A 162: 479-490.
Frixione, E., and H. Arechiga. 1981. Ionic dependence ofscreening
manuscript.
pigment migrations in crayfish retinal photoreceptors. / Comp.
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