Comparative Study of Temporal Resolution in the Visual Systems of Mesopelagic Crustaceans

8 Pages·1999·3.7 MB·English

by  T M Frank

Reference: Biol. Bull. 196: 137-144. (April 1999)
Comparative Study of Temporal Resolution in the
Visual Systems of Mesopelagic Crustaceans
TAMARA M. FRANK
Harbor Branch Oceanographic Institution, 5600 U.S. 1 N. Ft. Pierce. Florida 34946
Abstract. The temporal characteristics of the visual sys- trum and Stocker, 1952). These extracellular studies, using
tems ofeight species ofmesopelagic crustaceans were stud- the electroretinogram (ERG), which is the summed mass
ied using the electroretinogram (ERG). Experiments were response from a large number of receptor cells, were later
conducted on shipboard, using dark-captured specimens supported by studies on the intracellular responses ofsingle
collected offthe south coast ofCuba. As one would expect cells (Howard et ai, 1984; de Souza and Ventura, 1989).
based on the relative intensity differences in their light Since the light environment of mesopelagic crustaceans is
environments, the deepest living species. Systellaspis debi- similar to that of nocturnal insects, one might predict that
lis and Sergiofilictum, have low maximum critical flicker they would also have fairly low temporal resolution, and
fusion frequencies (CFFs) of 21-25 Hz. whereas the shal- that temporal resolution would be correlated with daytime
lowerliving species OploplwrusgracilirostrisandJanicella depth ofoccurrence. Although the spatial resolution, which
spinacauda have higher maximum CFFs (31-32 Hz). One is a function of the structure and optics of photoreceptors,
of the shallowest living species, Funchalia villosa, has an has been studied in a number of mesopelagic species (see
unusually low maximum CFF (24 Hz), which may be a Cronin, 1986; Land, 1990, for review), the temporal reso-
function of working with a dark-adapted eye. Two of the lution, which isafunction ofthe membranepropertiesofthe
bilobed euphausiid species, Nematobrachionflexipes andN. receptor cells themselves (see Weckstrom and Laughlin.
sexspinosus, have very high maximum CFFs (44-57 Hz), 1995, forreview), has received little attention. As shown by
comparable to those ofsurface-dwelling crabs, even though the theoretical analysis of Srinivasan and Bernard (1975),
they live between 400 and 600 m. The maximum CFF of visual acuity is dependent on both the spatial resolution and
Sprh\a-uIsoicihde,iriosn oinmliyxin3i6nniH.z,ainsdhiaclaltoiwnegrthlaitvinmgaxbiilmoubmedCeFuF- tihsemst,emvpisouraalltraersgoeltustiaorne orfartehleyesytea,tiboenacrayu.seEiftohrermotshte oorrggaann--
among the euphausiids cannot be correlated with depth of isms themselves are actively moving, so the environment is
occurrence. The unusually high flicker fusion frequency of in motion with respect to their photoreceptors, or their
the deeper living euphausiids may be correlated to their photoreceptors are moving because of muscle tremor or
preference for bioluminescent prey. nystagmus. Srinivasan and Bernard (1975) determined that
at angular velocities (of the object with respect to the
Introduction
organism viewing it) above a critical value, spatial resolu-
Autrum's studies of insect photoreceptors in the 1950s tion is more dependent on the temporal properties of the
gave risetothe ideathat the response dynamics ofthe retina photoreceptor cells than on the structural optics ofthe eye.
match the habitat and lifestyle of the organism. In these Therefore, for any comprehensive analysis of the visual
classic studies, he established that the eyes ofrapidly mov- system of an organism, both the spatial and temporal char-
ing day-active species have better temporal resolution, as acteristics of the photoreceptor need to be studied.
indicated by flicker fusion frequencies of200-300 Hz. than Studies on temporal resolution in mesopelagic organisms
the eyes of slower moving night-active forms, with flicker are rare, due to the difficulties in collecting visually com-
fusion frequencies of 10-20 Hz (Autrum, 1950, 1958: Au- petent organisms and keeping them alive during transport
back to shore-based labs. The only published study on the
Received 4 June 1998; accepted 9 December 1998. temporal characteristics of the visual systems of mesope-
137
138 T. M. FRANK
lagic organising is by Moeller and Case (1995), in which trawl fitted with a thermally insulated, light-tight closing
they demonslrated that two species ofdeep-sea crustaceans collecting container (cod-end). The light-tight cod-end was
have very low flicker fusion frequencies (8-12 Hz), com- closed at depth, ensuring that the organisms inside were not
pared to much higher maximum flicker fusion frequencies exposed to damaging light levels at the surface, as studies
(50-60 Hz) for shallow-water crabs (Brocker, 1935; Cro- have demonstrated that even low levels of light can cause
zier and Wolf, 1939). However, Moeller and Case (1995) permanent structural and physiological damage to the pho-
measured the critical flicker fusion frequency at threshold toreceptors of light-sensitive species (Loew, 1976; Nilsson
light intensities, which is difficult to compare between spe- and Lindstrom, 1983; Frank and Case, 1988b). Once at the
cies because (1) the threshold sensitivity ofacrustacean eye surface, the cod-end was detached from the net and carried
measured using the ERG technique varies considerably into a light-tight room, where it was opened and species
from preparation to preparation (pers. obs.), and (2) critical were sorted under dim red light. Specimens were main-
flicker fusion frequency is dependent upon the intensity of tained in chilled (8C), aerated seawater in 1-qt containers,
the stimulus light (Brocker. 1935; Crozier and Wolf, 1939; which were placed inside light-tight boxes. All trawling was
Croziere//., 1939). A lessproblematic characteristictouse conducted between the hours of 2200 and 0500.
for comparative studies of temporal resolution is the nia.\i-
nnini critical flicker fusion frequency. This is the maximum Electrophysiological recordings
ifnltiecnkseirtrya.teInthtahtetchuerreeynet isstucdayp,abtlhee mofaxfoilmluowmincgritaitcaalnyflilcigkhetr lenTghteh (stpheecieeusphianutshiiisdsstuadnydrJaannigceedllian ssipzienafcraoumd2a0) tmom80bmodmy
fusion frequencies ofthe photoreceptors ofeight species of
mme)sowpeerleageixcacmriunsetdaceuasnisngfrEoRmGa vraercioertdyinogfsd.epTthhes (re2s5u0lt-s90o0f bmooduynteldenognthan(aOcprlyolipchoprluassticgrhaocilldierrosatrnids).susTphenedyedwienrea
chilled (8C) seawater bath with the dorsal surface of the
these experiments indicate that several species from this
dfliimckelrigfhutsieonnvirartoens.meTnhtesheavuenussuuarplrliysihnigglhy rhaitgesh dmoanxoitmaupm- ewyheischjusatllaobwoevde tthheeirlevpelleoopfotdhse wtaoterre.maIinnthfisreceontfoigguernaetriaotne,
pear to be a function of depth of occurrence, but rather, respiratory water currents around the gills, the crustaceans
caepnpceearoftothbeepmroerfeerrceldosperleyy.correlated with the biolumines- HrlaeasmetariingnaenuddpaCtlooi.v1)e2awhn.adsAhpteluaanlcgtehsdytesfnuormbictcohrreoneedalulerlcayttriooindnetoh(fe1e0lxe/pfuet.rmeitymieep.:ntFAs.
Materials and Methods reference electrode was placed in the right eye, which was
then covered with black petroleum jelly (petroleum jelly
Animal collections mixed with black oil-based paint) to block all light input to
caobloTlahercedtectdrhueosfRtfaVctehSaeneswsoapuretdchiJecosohaunsssteodno,finCwiutthbhiasaso2tn.u4dayXr(eTs1a.eb8alrmechIT)curwcuekiresere atthhmiapstlibefyaiecc.aktgTirhooinu.snAddifnsfoieilrsveeenrtwicaahlslorsreuicbdoterrdaeiclntegecdttrfeorcdheonmgirqthuoeeunswdiagensdaluthsbeeefdwoars-eo
ter bath. Electrodes were placed in the eyes under dim red
light (>650 nm; Wratten Filter 79B). Signals were ampli-
fied with a Haer Microelectrode Amplifier (Model X
Table I
Cell-3) used in conjunction with a high-impedance probe to
Daytime ilcprh distribution ofcrustaceans in thi.\ eliminate electrode polarization artifacts (Kugel, 1977).
Low-frequency filters were set to minimal filtering (0.01-
Species Depth (ml* 0.1 Hz) to minimize distortion of the AC-amplified signal.
Family Euphausiacidae Data were digitized using a program written in LabView
Stylocheiron ^^n 250-500(1) (National Instruments, Inc.), and stored to disk for later
Nematobrachi* 400-600
(1) analysis.
Nematobrachion <l< \ipes 450-60011) This study was conducted on shipboard because the or-
Family Oplophoridae
./unicella spiiuu. 500-600(2) ganisms used will not survive transport to a shore-based
Oplophorusgraciliro 500-650(2) laboratory. Due to the difficulties inherent in working on a
Systellaspisdebilis 600-900(2) moving and rolling vessel, only extracellular electrophysi-
Family Penaeidae ology was possible.
Funchalia villosa 300-500(3)
Family Sergestidae
Set'gui filictum 600-900(4) Light stimuli
*Numbers in parentheses indicate the nurce of the data: (1) Roger, Test flashes of 490 nm light from an American Instru-
1978; (2) Hopkins </ al.. 1989; (3) Hopkins ,; /.. 1994; (4) Flock and ments SA monochromator (Model H-20) were delivered to
Hopkins, 1992. the eye via a fused silica light guide, positioned sothe circle
TEMPORAL RESOLUTION IN CRUSTACEAN VISION 139
oflight at the output was largerthan theeye. A piece oflens sponse latency is defined as the time from the start of the
tissue between the light guide and the eye served as a light stimulus to the start of the ERG.
diffuser. Flash duration was controlled by a Uniblitz shutter
(Model T132) undercomputercontrol, such that a50% duty Results
cycle (50:50 light:dark ratio) was maintained. Irradiance
was controlled with a neutral-density wheel driven by a The critical flicker fusion frequency measured via the
stepper motor undercomputercontrol, and calibrated with a extracellular electroretinogram is dependent on a variety of
UDToptometer (United Detector Technology Model S370) factors, namely adaptational state, background intensity,
and radiometric probe with point calibrations provided by stimulus intensity, and the subtended visual angle of the
UDT. source. In this study, all factors, with the exception of the
stimulus intensity, were equal for all the species: they were
all completely dark-adapted before being presented with a
Procedure flickering light stimulus, the background intensity was 0.
and the eye was always bathed with acircle oflightthat was
Although mesopelagic crustaceans are relatively insensi- larger than the eye itself. The only variable factor was the
tive to red light (Frank and Case. l"88a), the dim red stimulus intensity. Although the irradiance of the light
preparation light did produce a small degree of light adap- source was calibrated, the response to the light stimulus
tation. Therefore, after electrode placement, the specimen depended on the position ofthe electrode in the eye, so that
was dark-adapted until the response to a test flash, given a 100-|U,V response might be generated by a dim stimulus in
every 5 min, had not changed for 1 h, indicating that theeye one specimen and a brighter stimulus in another specimen
was in its fully dark-adapted condition. A flickering light of the same species. As shown in Figure 1, the CFF de-
stimulus of 1.5-s duration was then presented to the dark- pended on irradiance level, with lower irradiances evoking
adapted eye. To ensure that every flicker stimulus was lower CFFs and higher irradiances evoking higher CFFs.
presented to a fully dark-adapted eye, a dim 100-ms test Therefore, to ensure that the same parameter was measured
flash that elicited a 50-juV response (the smallest response forall species in this comparative study, the maximumCFF.
reliably discernible from background noise) in the fully which is the highest flicker rate that the eye is capable of
dark-adaptedeye was presentedtotheeye afterevery flicker following at any intensity, was used.
stimulus, and the eye was allowed to re-dark-adapt until the
test flash response had recovered to 50 /J.V, before the next Maximum criticalfusionfrequency
flicker stimulus was presented. The flicker rate for subse- The maximum CFFs were measured for eight species of
quent stimuli was increased until critical flicker fusion was mesopelagic crustaceans from a variety ofdepths (Table I).
achieved; this isdefined as thepoint at which theeye can no
longerproduce a modulated electrical signal that remains in
phase with the flickering light. Irradiance was then in- Oplophorus qracilirostris
creased by one log unit, and the flicker rate ofthe stimulus
^
light was increased until fusion was again achieved. Maxi-
mum
critical flickerfusion frequency (CFF) is definedas the
point at which furtherincreases in irradiancedo notresult in
a faster flicker fusion frequency. All maximum CFFs are in
reference to dark-adapted eyes.
The responses to single 100-ms flashes of490-nm light of
varying irradiances were also measured, starting from irra-
diances generating a threshold response, and continuing to
the point at which further increases in irradiance produced
no further increases in response amplitude. In some prepa-
rations, the response was not saturated at the maximum
stimulus light irradiance. For those preparations in which
response saturation was reached, the log 110was determined;
this is the log ofthe stimulus irradiance eliciting a response
that is 10% of the maximum amplitude. The log ll() was
used as an estimate of the relative sensitivity of the photo-
receptors (after de Souza and Ventura, 1989).
Forall species, latencies were measured using a response
amplitude that was 10% of the maximum response. Re-
140 T. M. FRANK
Three species, Sergiafilictum, Systellaspisdebilis, and Fun-
chciliu rillosa. had relatively low maximum CFFs, between Systellaspis debilis
20 and 25 Hz (Table II), as one would expect from species
coming from avery low light environment. A representative
example of an ERG is shown for Systellaspis debilis in
Figure 2A. Three species, Oplophoms gracilirostris, Juni- 20
cella spinacauda, and Stylocheiron maximum, had some-
what higher rates, between 31 and 36 Hz; and two species,
Nematobrachionflexipes and Nematobrachion sexspinosus,
22 HZ
had extremely high CFFs. considering their dim light envi-
ronment, of44 and 57 respectively (Table II). A represen- B
tative example of an ERG for N. sexspinosus is shown in
Figure 2B. Nematoscelis sexspinosus
ERG
Sensitivity
The overall sensitivity of the eye was estimated by de- S AAMlWimilMAJMlMIWlJl
termining the log of the irradiance (log I,,,) required to
produce a response that was 10% of the amplitude of the
maximum response the eye was capable of generating. In ERG
several preparations, the maximum response was not seen,
and the log 1,,, could not be determined. As shown in Table S 63 Hz
II, there is a trend towards lower sensitivity to light as the
response dynamics of the eye speeds up. Systellaspis debi-
lis, the species with the lowest maximum CFF. had, accord- ERG
ing to the log llo, the most sensitive eye, while N. sexspi- S 65 Hz
nosus, the species with the highest maximum CFF, has the
lowest sensitivity to light. Figure 2. Representative examples of species with low and high
flickerfusionfrequencies. ERGdesignates theresponserecorded fromthe
Response latency eye;Sdesignatestheflickeringlightstimulus.Thedatashownarefromthe
As an indicator of the speed of transduction in the pho- wlaasst0a.b4lestoofftohlelo2w-sthsetismtuilmuuslupsullsieg.ht(Aat)2T0heHzEcRyGclefrfoomrcSyycsltee;l/aatsp2i2sHdze.bitlhies
toreceptors of the various species, latency from the start of ERGresponsewaslaggingbehindthelightstimulusand"missing"cycles.
the light stimulus to the start ofthe photoreceptor response (B) The ERG from Nematoscelis sexspinosus was able to follow the
was measured, using a response amplitude that was 10% of stimulus lightat60Hz. At63 Hz.theERGappearstobeinphasewith the
stimulus light,butcareful examinationofthedatashowsthat 25 flashesof
light weregiven,butonly 23 responses wereproduced. By65 Hz, the lag
isevengreater, andthe ERG isclearly "missing" cycles. TheCFFofthis
Table II specimen is 60 Hz. since this is the last recorded frequency at which the
Mean valuesfortemporal resolution (max CFF). sensitivitv (Log llu) ERG was able to match, cycle forcycle, the phase ofthe stimulus light.
ami response latencies obtainedfrom ERG data
the maximum amplitude. Species with lower flicker fusion
Species Max CFF IH/J (photonLsogcmI1"0- s~'I La(tmesn)cy frequencies also have longer latencies, indicative of slower
eyes, and species with higherflickerfusion frequencies have
=
SFyusntcehlalalsipaisw7d/e,b.iwl.ix 2241 ((0.0.56;;nn = 42)) 98..39((0.0.00)6) 5785((2.6.09)) eyes with much faster response dynamics (Table II).
Sergiafilictum 15(n = 1) NA NA
Janicella spinacat,. (0.3;n = 3) 9.4(0.06) 49(3.5) Discussion
Oplophoms
gracilirostris '. n = 2) 9.4(0.09) 42(5.5) The vertical distributions ofthe species examined in this
Stylocheironmaximum 36(n 10.0 42 study have not been determined forthe south coast ofCuba.
Nematobrachion The vertical distribution data in Table I are for the Gulf of
flexipes 44( I (). /, >) 10.2 ( 0.38) 22( 0.5) Mexico, except for the euphausiids. Since Gulf of Mexico
Nematobrachion
sexspinosus 56(2.0;n = 4) 10.8(0.18;n = 2) 16(2.5) wboattheraroeraisgihnaatveesJienrltohve'sCTaryipbebe1aonrS1eAa w(aNtoewrli(nJ,erl1o9v7.1)1,97a6n)d.
SpeciesarerankedbymaxCFF.from lowesttohighest. Standarderrors it is likely that these two areas would have similar species
and numberofspecimens tested are in parenthesis. assemblages anddistribution patterns. The abundance ofthe
TEMPORAL RESOLUTION IN CRUSTACEAN VISION 141
three species ofeuphausiids in this study wasextremely low MaximumCFFvs.Depth
intheGulfofMexico (Kinsey and Hopkins, 1994), as itwas
off the coast of Cuba (pers. obs.). and comprehensive data 60
on depth distribution are not available for these areas. The N. sexspinosus'
data presented in the table are forthe tropical Pacific, where
Jerlov's Type 1 or 1A water is also present. The depth
distributions ofnine relatively abundant euphausiid species 50 -
in the Gulf of Mexico (Kinsey and Hopkins. 1994) were
compared withthoseprovidedby Roger(1978) forthe same
N. flexipes
species in the tropical Pacific, and the depth ranges proved
40 -
to be the same in the two areas. Therefore, it is likely that
the data presented for the vertical distribution of Nemato- S maximum
brachion flexipes, N. se.\spinosus, and Stylocheiron maxi- O.gracilirostris
mum in the tropical Pacific would also apply to the Gulfof 30 - J spinacauda
Mexico.
Depth vs. criticalflickerfusion F. villosa S. filictum
20 S. debilis
Shallower depth ranges do not necessarily mean a
brighter light environment: an organism found at 300 m in
murks water might see significantly less light than an or-
ganism found at 500 m in very transparent water. However, 10 -
in this study, the depth of occurrence is an indication of
relative light intensity, as the water is all Jerlov's Type ! or
1A (Jerlov. 1976). Most of the species in this study live
below 400 m. At 400 m during the day. in Jerlov's type 1
water, downwelling ambient light has been reduced to less 200 300 400 500 600 700 800 900 1000
than 0.0001% ofthe surface irradiance (Jerlov, 1976). This DaytimeDepth(m)
is aboutasbrightas the moonlight seenby nocturnal insects, Figure3. Maximumcritical flickerfusion frequency(CFF)asafunc-
in that light from a full moon is 0.0001% of daytime tion ofdaytime depth distribution for the eight species in this study.
illumination (Munz and McFarland, 1973; Land. 1981).
Therefore, one would expect mesopelagic crustaceans to flicker fusion frequency would result from such a dim light
have relatively low maximum CFFs. indicative oflow tem- stimulus.
poral resolution, as has been found in nocturnal insects At first glance, the very low maximum CFF of the
(Autrum. 1950, 1958, 1984; Howard et al.. 1984: de Souza penaeid. Funclmlia villosa, is somewhat puzzling. It is one
and Ventura. 1989; Laughlin and Weckstrom, 1993). In of the shallowest living species, and also possesses an eye
addition, one might expect the deepest dwelling species, with a fairly high spatial resolution (Herring and Roe.
which live in the dimmest light, to have the lowest maxi- 1988). High spatial resolution is usually correlated with a
mum CFFs. This is certainly the case for the two deepest higher light environment, and is also associated with a
living species in this study an oplophorid, Systellaspis comparatively higher temporal resolution (Srinivasan and
debilis, and a sergestid. Sergiofilictum which have max- Bernard, 1975). However, these measurements ofmaximum
imum CFFs of20-25 Hz (Fig. 3). equivalent to those ofthe CFF were made in a completely dark-adapted eye; the eye
nocturnal slow moving insects studied by Autrum (1950. of F. villosa, which is of the superposition type, possesses
1958). Oplophorus gracilirostris and Janicella spinacauda migrating screening pigments, which changes the eye from
are in the same family as S. debilis. but have higher maxi- a spatially acute, apposition-like eye during the day to an
mum CFFs between 31-32 Hz. Theirdaytime depthrange eye with less spatial resolution, but greater sensitivity, at
is about 100 m shallower than that ofS. debilis (Fig. 3). so night (Herring and Roe. 1988). Maximum CFF is known to
a highermaximumCFFis not unexpected. A previous study be higher in the light-adapted vs. the dark-adapted eyes of
by Moeller and Case (1995) reports a critical flicker fusion shallow-water crustaceans that possess mobile screening
frequency of 12 Hz for Oplophorus spinosus, which has a pigments (Crozier and Wolf. 1939; Crozier et al.. 1939:
depth distribution similar to that of O. gracilirostris. How- Brocker, 1935). but mobile screening pigments are usually
ever, those authors were using a light that was only 1 log not found in mesopelagic species (see Hallberg and Elofs-
unit above the irradiance that produced a threshold re- son. 1989. forreview). F. villosa appears to be anexception
sponse, and as shown by Figure 1. a much lower critical to this rule. Looking at the other species in this study, the
142 T. M. FRANK
screening pigments in the photoreceptors of Oploplwrus Criticalflicker fusion and bioluminescence
spinosus (Welsh and Chace. 1937; Land, 1976; Gaten etai,
1992). a close relative of O. gracilirostris with the same Although the crustaceans in this study share the same
depth distribution, and Systellaspis debilis (Gaten el ai, light regime as nocturnal insects with respect to background
1992) do not appearto be mobile. Although some species of illumination, many oftheir prey are bioluminescent. Biolu-
sergestids may possess screening pigments (Welsh and minescence, which is very rare in the terrestrial environ-
Chace, 1938), it is not known whether these are mobile. ment, is an extremely common phenomenon in the oceanic
Chun (1896). Zimmer (1956), and Meyer-Rochow and realm. In the mesopelagic zone (200-900 m), luminescence
Walsh (1978) found noevidence ofthe migration ofscreen- has been found in upto 75% ofthe fish species (Herring and
ing pigments in euphausiid eyes, and while Kampa (1965) Morin, 1978) and 79% of the shrimp species (Herring,
indicates that some migration does occur. Land etal. (1979) 1976). Nocturnal terrestrial insects must image dark objects
conclude that this migration is notofsufficient magnitude to against a dimly lit background, so a higher temporal reso-
affect the spatial resolution ofthe eye. It remains to be seen lution, with the resulting decrease in contrast sensitivity,
whetherF. villosa, whose spatial resolution is clearly higher wouldbe aconsiderable disadvantage. In theocean, itmight
when its screening pigments are in the light-adapted posi- be advantageous for predatory carnivorous species to sac-
tion, will also demonstrate a higher temporal resolution rifice sensitivity for the ability to more accurately track a
under light adaptation that is more consistent with its day- glowing or flashing prey item.
time depth distribution. Future studies will include deter- All euphausiid species with bilobed eyes possess an ex-
mining the temporal resolution ofF. villosa, as well as that tremely elongated second or third thoracic leg, some with
ofother species without migrating screening pigments, un- clawlike chelae at the end, which is hypothesized to be an
der light-adapted conditions. adaptation for active carnivorous feeding (Mauchline and
The three euphausiid species in this study (Nematobra- Fisher, 1969). If some of these species specialized in cap-
chion sexspinosus, N.flexipes, and Stylocheiron maximum) turing bioluminescent prey, the greater contrast between a
all have bilobed eyes, and Chun (1896) determined (mor- bioluminescent prey item against a dim background vs. a
phologically) that the upper lobe, which is oriented upwards dark prey item against a dim background would make it
toward the brighter downwelling light, has higher spatial advantageous for these species to sacrifice sensitivity (and
resolution than the lowerlobe, which isorienteddownwards hence contrast detection) in return for greater temporal
towards dimmer upwelling light. Due to limitations set by resolution (and hence tracking ability). This rationale would
working on shipboard, the responses from receptor cells in likewise explain the puzzling result that Stylocheiron max-
the upper lobe could not be isolated from responses from imum, which is also a bilobed euphausiid with an elongated
receptor cells in the lower lobe. Therefore, it remains to be thoracic appendage, has the shallowest depth distribution of
determined whether the temporal resolution differs between the three euphausiid species but also the lowest maximum
the two lobes. However, it is clear that two ofthese species. CFF (Fig. 3). S. maximum eats primarily copepods in the
N. sexspinosus and N. flexipes, have the highest maximum genera Oithona. which is nonluminescent, and Oncaea, of
CFFs of all the species in this study, comparable to CFFs which only one species is known to be bioluminescent (see
reported for shallow-water crabs (Brocker, 1935; Crozier Herring, 1985, for review), and this bioluminescent species
and Wolf. 1939). This is unexpected, because their daytime is not present in the Gulf of Mexico (Kinsey and Hopkins,
depths of occurrence are in the middle of the depth distri- 1994). Since the biomass and species distribution off Cuba
bution for the eight species in the study (Fig. 3). These two is similar to that of the Gulf of Mexico, it is likely that 5.
species live at a depth at which the downwelling light maximum is eating primarily nonbioluminescent prey in
intensity is roughly the same as that experienced by noc- Cuban waters as well. On the other hand, the primary prey
turnal insects under a full moon (see above), yet they have item ofN. sexspinosus and N. flexipes. the two species with
asubstantially highermaximum CFF(40-60 Hz) than most the highest critical flicker fusion frequencies, is an active
nocturnal insects (10-20 Hz; Autrum. 1950, 1958). Laugh- bioluminescent copepod called Pleuromamma (Hu. 1978;
lin and Weckstrom ( 1993) demonstrated that the benefits of Kinsey and Hopkins, 1994). all species ofwhich emit some
high temporal res; ion are limited fornocturnal, generally form of bioluminescent spew (see Herring, 1985. for re-
slow moving insects, and that the metabolic price for im- view). To further support the argument that this visual
proving the temporii! hh of vision is substantial. In adaptation is driven by bioluminescence, the Nematobra-
addition to the metabolic < ., ''ise, fast photoreceptors have chion species, as mentioned above, have a deeper depth
a lower sensitivity than slow photoreceptors (Laughlin, range than S. maximum, but possess a less sensitive eye,
1990). which would be a distuu Disadvantage to organisms according to the log ll() values (Table II). Following Au-
living in a light-limited environment. However, these con- trum's hypothesis, one would predict that the organism
clusions were drawn for terrestrial organisms, and other from the dimmer light regime would have the more sensi-
factors must be taken into account in the oceanic realm. tive eye with slower response dynamics (assuming similar
TEMPORAL RESOLUTION IN CRUSTACEAN VISION 143
activity levels). However, because theNematobrachion spe- and crew of the RV Seward Johnson for their great assis-
cies are specializing in bioluminescent prey, the advantages tance with animal collection. I alsothank Dr. Simon Laugh-
of a higher temporal resolution might outweigh the advan- lin forhis valuable advice, and Dr. Edith Widder, Dr. Sonke
tages of a more sensitive eye. Johnsen. and Ms. Erin Fisher fortheir helpful comments on
Otherspecies, however, might benefit fromhaving aneye the manuscript. Additional funding for this work was pro-
with lower temporal resolution. Ifthe preferred biolumines- vided by NSFGrant No. #OCE-9313972 toT. M. Frank and
cent prey were a slow moving item that glowed, such as E. A. Widder. Harbor Branch Oceanographic Institution
some species of gelatinous zooplankton, or marine snow Contribution #1270.
colonized by bioluminescent bacteria, an eye with a lower
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