Visual physiology of the Antarctic amphipod Abyssorchomene plebs.
Visual systems may be uniquely adapted structurally and physiologically to the light environment in which they must function (reviewed in Lythgoe, 1979). Structural adaptations include modifications to dioptric elements, to photoreceptor arrangement, and to presence or absence of tapetal reflectors, while physiological adaptations may be to spectral (wavelength) sensitivity, absolute irradiance sensitivity, and temporal resolution (reviewed in Land and Nilsson, 2002). Often, these adaptations are trade-offs. For example, all else being equal, a fast eye with high temporal resolution will not be as sensitive to light as a slower eye that is capable of sampling photons over a longer time interval (Warrant, 1999).
One environment in which visual adaptations have received considerable attention is the deep sea. Many animals living at mesopelagic depths (200-1000 m) have eyes efficient at capturing both the dim downwelling light and luminescence from other organisms (reviewed in Warrant and Locket, 2004). Crustaceans are quite successful at these depths and posses a wide range of eye designs and physiological abilities to capture prey, avoid predators, and find mates in low light (reviewed in Marshall et al., 2003).
Because of its low light levels and stable cold temperatures, the mesopelagic is similar in many ways to shallower benthic habitats of polar oceans, a region where some crustacean groups, most notably the amphipods, are quite successful (reviewed in Arntz et al., 1994). Although the metabolic adaptations of polar and deep-sea crustaceans are often similar (Vetter and Buchholz, 1998), too little is known about the sensory capabilities of polar crustaceans to assess whether the sensory adaptations are also similar. Accordingly, a characterization of the visual adaptations in crustaceans from polar habitats would be instructive, both for understanding how neural systems function in extremely cold environments and for further characterizing the ecological role of vision in dim habitats.
In this study, we examined aspects of the visual physiology of the Antarctic amphipod Abyssorchomene plebs (Hurley, 1965) (Gammaridea: Lysianassoidea). This species is a common benthic scavenger that lives at depths from 10 to 800 m and has a circumpolar distribution (Rakusa-Suszczewski, 1982; Nyssen et al., 2005). Meyer-Rochow and Tiang (1979) described the compound eye of A. plebs, which has about 260 ommatidia with the five retinular cells per rhabdom typical of other amphipods (Hallberg et al., 1980). To characterize basic aspects of visual function in A. plebs, we determined photoreceptor spectral sensitivity, irradiance sensitivity, and temporal resolution electrophysiologically at 3 [degrees]C. Because the retinal screening pigments of A. plebs have been shown to migrate upon light adaptation at 0 [degrees]C as well as in the absence of light when the temperature is raised 10 [degrees]C (Meyer-Rochow and Tiang, 1979), we also tested the effect that light adaptation and a 4 [degrees]C temperature increase (to 7 [degrees]C) in the dark had on irradiance sensitivity and temporal resolution.
Material and Methods
Specimens of Abyssorchomene plebs (Fig. 1). were collected in February 2006 from McMurdo Sound, Antarctica (77[degrees] 50.885' S, 166[degrees] 39.533' E) at a depth of about 18 m off McMurdo Station. A canvas bag baited with frozen fish (Trematomus bernacchii) was lowered to the bottom through an ice hole and recovered after about 24 h. Scavenging individuals were picked from the fish and immediately placed in light-tight containers and maintained overnight at 4 [degrees]C. Although brief exposure to the relatively bright surface light may have slightly damaged their photoreceptors, they should have recovered prior to experiments (Meyer-Rochow and Tiang, 1979). Specimens were transported in darkness at 4 [degrees]C over the next 4 days to the Harbor Branch Oceanographic Institution (Fort Pierce, Florida), where all experiments were conducted. At Harbor Branch, the amphipods were maintained without feeding in darkness at 1 [degrees]C with periodic changes of seawater. No mortality was observed during transport or over the following 2 weeks of experimentation.
The spectral sensitivity, irradiance sensitivity, and temporal resolution of the photoreceptors were determined electrophysiologically by recording electroretinograms (ERGs). Under dim red light, live specimens of A. plebs (non-ovigerous females; mean length = 14.7 [+ or -] 2.2 mm, SD) were attached dorsally to the plastic head of a pin with cyanoacrylate gel adhesive (Loctite Corp.), and mounted in an acrylic support within a chilled seawater bath (0-3 [degrees]C, except where indicated below). Water level was adjusted such that about one-quarter of the animal's eye was in air above the water surface while the rest of the eye and the body were submerged in water with a temperature gradient of 3 [degrees]C at the surface, decreasing over 1 cm to 0 [degrees]C. Thus, the experimental temperature was considered to be 3 [degrees]C. Although we attempted to conduct the experiments closer to the ambient temperatures of McMurdo Sound (-1.86 [degrees]C; Arntz et al., 1994), we encountered problems in maintaining the bath at that temperature in a 24 [degrees]C room. In the described preparation, the amphipods remained alive and active during experiments lasting up to 4 d. Single-ended ERGs were made by placing a metal microelectrode (13-15 m[ohm]; FHC Inc.) subcorneally in the portion of the eye above the water, and grounding the seawater bath with an AgCl-coated wire. A.C. recordings were digitized and stored in LabView, ver. 6.1 (National Instruments) for later analysis of peak-to-peak response heights.
The monochromatic stimulus light (Spectral Products, model CM110 monochromator) was directed onto the eye of the specimen via one branch of a bifurcated, randomized fiber optic light guide (EXFO). In this way, the whole eye was bathed in diffuse light, although all ommatidia were not likely to have been uniformly stimulated. A Uniblitz shutter (model VS25) provided a stimulus flash duration of 75 ms, and stimulus irradiance was adjusted using a neutral-density wheel driven by a stepper motor, both of which were under computer control. Irradiance was calibrated at 10-nm intervals with a photometer (UDT Instruments, model S370) using a calibrated radiometric probe. Spectral purity at test wavelengths without the use of blocking filters was verified by a spectroradiometer (~15-nm FWHM (full width half maximum), 320-700 nm; Optronic Laboratories, model OL754). A fiber optic illuminator (Dolan-Jenner, DC-950) connected to the other branch of the light guide provided accessory illumination during electrode placement and chromatic adaptation experiments. White light from the lamp was filtered for electrode placement using an orange longpass filter (Melles Griot, OG590), and for adaptation to selected wavelengths (chromatic adaptation) using interference filters (381-nm, Ealing #35-3458, 14-nm FWHM; 478-nm, Ealing #35-3094, 14-nm FWHM). Irradiance of the adapting light was controlled by neutral-density filters.
Spectral sensitivity experiments
Spectral sensitivity experiments (n = 8) began when the response to a dim test flash had remained constant for 1 h, indicating the eye was dark adapted. Spectral sensitivity of the dark-adapted eye was determined by stimulation with 75-ms test flashes of monochromatic light and adjusting irradiance to reach a defined criterion response at each wavelength tested (330-630 nm). The criterion response was either 40 or 50 [micro]V, which was about 20 [micro]V above background noise for each preparation. A test flash of standard wavelength and irradiance was periodically given throughout the experiment to confirm that the eye remained dark adapted and was not affected optically due to prolonged air exposure. If the response to test flashes was variable for a given preparation, further experiments were not conducted, and previous experiments on that animal were not used in analyses. Chromatic adaptation experiments were conducted after the dark-adapted spectral sensitivity was determined by light-adapting the eye at either 381 nm (UV, n = 3) or 478 nm (blue, n = 4), waiting until a constant response to a dim test flash was observed for 1 h, then re-testing spectral sensitivity at all wavelengths. Irradiance of the adapting light was set to reduce the sensitivity of the eye by 1 log unit at the adapting wavelength.
Data for the spectral sensitivity of dark-adapted animals were plotted as the reciprocal of the irradiance required to evoke the criterion response at each wavelength, and normalized to the wavelength of maximum sensitivity. Templates for A1-based visual pigment (rhodopsin) absorbance (Govardovskii et al., 2000) were used to calculate the absorptance curve that produced a minimum sum of squares fit to the spectral sensitivity data (Stavenga et al., 1993). To achieve this best fit, values for [[lambda].sub.max] and visual pigment specific absorbance were optimized, while rhabdom length was assumed to be 54 [micro]m (measured from fig. 2B in Meyer-Rochow and Tiang, 1979).
Irradiance sensitivity experiments
Irradiance sensitivity was determined by presenting 75-ms light flashes of varying irradiance and measuring the magnitude of the ERG. The wavelength of maximum sensitivity (480 or 490 nm) determined for a given dark-adapted animal in the spectral sensitivity experiment was used to determine that specimen's irradiance sensitivity. Each subsequent stimulus flash was not presented until the response to a dim test flash (as described above) had recovered to dark-adapted levels. Irradiance sensitivities of four specimens were tested at 3 [degrees]C, and for two of these specimens, the temperature was raised to 7 [degrees]C and the experiment repeated. This temperature is higher than A. plebs would experience in nature but lower than its upper lethal temperature (8 [degrees]C; Rakusa-Suszczewski, 1982). Examining visual physiology at abnormally warm temperatures is of interest given that structural changes in A. plebs photoreceptors similar to those occurring during light adaptation occur in response to such temperature increases (Meyer-Rochow and Tiang, 1979). Irradiance sensitivity for a single specimen at 3 [degrees]C was also tested after chromatic adaptation with 381 and 478 nm light as described above.
Peak-to-peak ERG amplitudes (V) were measured and modeled as a function of log irradiance (log I), using the Zettler modification of the Naka-Rushton equation (Naka and Rushton 1966a,b; Zettler, 1969; Frank, 2003). The model slope (m) and the log irradiance evoking 50% of the maximum response amplitude (log K) were calculated to provide an estimate of sensitivity for the A. plebs eye (Barth et al., 1993; Frank, 2003). The eye's dynamic range, defined as the log irradiance range evoking 5%-95% of the maximum response amplitude, was also calculated as a measure of photoreceptor sensitivity (Laughlin and Hardie, 1978).
Temporal resolution experiments
Temporal resolution of the A. plebs eye was quantified using two methods: (1) response waveform dynamics, and (2) flicker fusion frequency. Waveform dynamics of the ERGs in response to individual flashes of light were analyzed for (a) response latency, defined as the amount of time elapsed from the onset of the light stimulus until the onset of the photoreceptor response, and (b) time-to-peak, defined as the amount of time elapsed from the onset of the light stimulus until the peak response. Both parameters were calculated from flashes yielding response amplitudes about 10% of the maximum amplitude, as determined from the V/log I curves (Frank, 1999, 2003). Response latency and time-to-peak were determined for dark-adapted specimens at 3 [degrees]C (n = 4) and 7 [degrees]C (n = 2).
Flicker fusion frequency experiments involved presenting the eye with square pulses from a flickering stimulus light, generated by cycling a computer-controlled electromagnetic shutter in the light path, for 2 s at a given frequency with a 50:50 light/dark ratio, and recording the corresponding ERG (see Frank, 1999). The frequency at which the eye could no longer respond to individual light flashes over a 0.5-s interval was defined as the critical flicker fusion frequency (CFF). As the irradiance of the stimulus light is increased, CFF increases to a maximum and then plateaus (Glantz, 1968). Experiments began by determining CFF for the irradiance evoking an ERG amplitude 20-[micro]V above background noise. CFF was then determined for 0.5-log increases in irradiance until three successive irradiance increases did not result in CFF increases, providing a maximum CFF value. Test flashes of dim light (as described above) were given after each stimulus train to ensure that the eye recovered to its initial state of adaptation before the next stimulus train was presented. Experiments were conducted on seven dark-adapted specimens at 3 [degrees]C, five of which were again tested under light-adaptation (478 nm) at 3 [degrees]C. Three specimens tested under both light and dark adaptation at 3 [degrees]C were also tested under dark adaptation at 7 [degrees]C.
The spectral sensitivity function for dark-adapted specimens of Abyssorchomene plebs shows a major peak in the blue, with a minor sensitivity peak in the ultraviolet (UV). The best-fit visual pigment absorptance curve has a [[lambda].sub.max] of 487 nm and visual pigment specific absorbance of 0.013 [micro][m.sup.-1] (residual sum of squares = 0.123) (Fig. 2). Chromatic adaptation with either 381 nm (UV) or 478 nm (blue) light resulted in a loss of visual sensitivity (Fig. 3A), yet the ratio of mean UV response (350, 370, and 390 nm) to mean blue response (470, 480, 490, and 510 nm) remained constant and equal to that of dark-adapted individuals (P = 0.371, one-factor repeated measures ANOVA) (Fig. 3B). Wavelength-specific changes in response waveforms (e.g., Frank and Case, 1988) did not occur during chromatic adaptation experiments.
V/log I data for dark-adapted animals at 3 [degrees]C (n = 4) were sigmoidal and modeled using the Naka-Rushton equation (Fig. 4A). Parameters derived from the model fit that quantify the irradiance sensitivity of A. plebs are slope (m; 0.569), log K (11.75 log photons [cm.sup.-2] [s.sup.-1]), and dynamic range (4.49 log photons [cm.sup.-2] [s.sup.-1]). Two dark-adapted specimens were tested at both 3 and 7 [degrees]C (Fig. 4B), with only minimal change in model parameters with the temperature increase (for 3 and 7 [degrees]C, respectively: m = 0.687, 0.763; log K = 12.2, 12.13 log photons [cm.sup.-2] [s.sup.-1]; dynamic range = 3.72, 3.35 log photons [cm.sup.-2] [s.sup.-1]).
A single specimen was tested at both 3 and 7 [degrees]C while dark adapted, and at 3 [degrees]C while light adapted to UV and blue light (Fig. 4C). These data were plotted as actual ERG amplitudes, and not normalized to V/[V.sub.max], in order to maintain differences present under the treatments. Light-adapted curves at 3 [degrees]C are shifted to higher irradiances relative to dark-adapted curves at both 3 and 7 [degrees]C. Accordingly, log K values for dark-adapted specimens at 3 and 7 [degrees]C were 12.7 and 12.61 log photons [cm.sup.-2] [s.sup.-1], respectively, while light-adapted specimens at 3 [degrees]C had larger log K values of 13.16 (UV adapted) and 13.49 (blue adapted). However, the functional form of the V/log I curves remained the same for all treatments with this specimen; model slopes (m) were from 0.722 to 0.796, and dynamic ranges were from 3.22 to 3.55 log photons [cm.sup.-2] [s.sup.-1], showing no apparent trend with light adaptation.
Waveform dynamics (response latency and time-to-peak) were calculated for light flashes evoking 10% of the maximum V/log I response. A significant difference is present in both the response latency (P = 0.012, two-sample Student's t-test) and time-to-peak (P < 0.001, two-sample t-test) for dark-adapted individuals at 3 [degrees]C relative to those at 7 [degrees]C, with a delayed response at the colder temperature (Fig. 5; Table 1). Likewise, maximum critical flicker fusion frequency (CFF) increased with an increase in temperature, having a [Q.sub.10] of 1.92 (Fig. 6; Table 1). Maximum CFF values were significantly less for dark-adapted individuals at 3 [degrees]C (11.7 Hz) than at 7 [degrees]C (15.0 Hz) (Fig. 6), yet neither of these treatments yielded results significantly different from those for animals adapted to blue light at 3 [degrees]C (14.0 Hz) (Table 1; P = 0.006, one-factor ANOVA; pairwise comparisons using the Holm-Sidak test).
The spectral sensitivity of Abyssorchomene plebs was preliminarily investigated by Meyer-Rochow (1980), who observed a sensitivity maximum between 474 and 513 nm by using an in vivo optical method. Similarly, our electroretinograph data suggest a blue spectral sensitivity maximum of 487 nm for A. plebs. Visual spectral sensitivities around this wavelength region are typical of open-ocean crustaceans, including Antarctic krill (Euphausia superba), whereas coastal-dwelling crustaceans often have longer sensitivity maxima (Frank and Widder, 1999; Johnson et al., 2002; reviewed in Marshall et al., 2003). For example, the coastal Arctic amphipods Pontoporeia affinis and P. femorata have spectral sensitivity maxima in the green at 550 nm (Donner, 1971).
Visual spectral sensitivities are often interpreted as ecological adaptations to light conditions that maximize photon capture or enhance visual contrast in a specific habitat or for a specific behavioral function (reviewed in Lythgoe, 1979; Marshall et al., 2003). The spectral composition of light at benthic habitats of McMurdo Sound is not well characterized and depends in part on water column depth and clarity (e.g., amount of colored dissolved organic material), as well as on physical and biological aspects of the overlying sea ice. Broad-spectrum sunlight is filtered first by snow and ice, then by seawater, both of which maximally transmit blue light of about 475 nm (Maykut and Grenfell, 1975; Arrigo et al., 1993). If high concentrations of land-derived organic material or phytoplankton are present in the ice or water, the spectral maximum of transmitted light is shifted to longer green and yellow wavelengths (Arrigo et al., 1993; Robinson et al., 1995). This shift may not be as dramatic in Antarctic coastal water as it is elsewhere, because without major rivers, land-derived organic inputs are limited to glacial ice deposits (Isla et al., 2006). The observed spectral sensitivity of A. plebs at blue wavelengths with substantial sensitivity in the UV fits with its occurrence over a wide range of seafloor depths in McMurdo Sound (10-800 m; Rakusa-Suszczewski, 1982). As this species may exhibit ontogenetic and seasonal vertical migrations (Rakusa-Suszczewski, 1982), further study of its spectral sensitivity with stage and season may be interesting, as would detailed study of the spectral quality of its habitat.
A curious feature of the spectral sensitivity function for A. plebs is high sensitivity in the UV-A (350-390 nm) (Fig. 2). Some sensitivity in this region is expected due to the [beta]-band of the rhodopsin molecule (~20% of the [[lambda].sub.max] [alpha]-band; Stavenga et al., 1993), but A. plebs is more sensitive in this region than predicted by the rhodopsin template, and its sensitivity is shifted to longer wavelengths (370-nm maximum). While these features suggest that a second visual pigment may be present, the lack of wavelength-specific waveform changes and chromatic adaptation effects (Fig. 3) does not support a dichromatic visual system in A. plebs; adaptation to both 381- and 478-nm light resulted in similar losses of sensitivity at both UV and blue wavelengths. Similar findings from electroretinography of the land crab Gecarcinus lateralis (Lall and Cronin, 1987) and the ctenid spider Cupiennius salei (Barth et al., 1993) were interpreted as resulting from multiple visual pigments. An alternative, though unlikely, hypothesis to a dichromatic visual system for explaining the heightened UV sensitivity of A. plebs is that a UV-absorbing pigment transfers quantal energy to a rhodopsin/metarhodopsin absorbing at longer wavelengths (e.g., Minke and Kirschfeld, 1979; Hamdorf et al., 1992). It is not possible from the present data to determine if a UV-sensitizing pigment hypothesis could explain the UV sensitivity of A. plebs, but intracellular recording and microspectrophotometry would help to evaluate this possibility. All data at present suggest that A. plebs has a monochromatic visual system (sensu Marshall et al., 2003).
While it is not possible to use electroretinography for determination of absolute sensitivity to light (see Frank, 2003), relative comparisons can be made with other studies using similar techniques, although it is possible that differences among organisms in neural architecture may affect the recordings. The dynamic range of the dark-adapted A. plebs eye is 4.49 log photons [cm.sup.-2] [s.sup.-1] at 3 [degrees]C, which fits with the value of about 4 log units commonly observed for arthropods from a range of habitats (Laughlin and Hardie, 1978; Barth et al., 1993; Frank, 2003). The log K for dark-adapted specimens of A. plebs (11.75 log photons [cm.sup.-2] [s.sup.-1]) is most similar to that of crustaceans from the deep sea; for a variety of deep-sea crustaceans, log K values determined using the same methods described in this study are 10.31-12.21 log photons [cm.sup.-2] [s.sup.-1] (Frank, 2003), while for the semi-terrestrial crabs Uca thayeri and U. pugilator, which live in a much brighter light environment, log K is higher (13.9 and 14.8 log photons [cm.sup.-2] [s.sup.-1]; N. McMullen, Florida Atlantic University, unpubl. data). Downwelling irradiance on the seafloor at the collection site (18 m) with overcast skies during austral summer (25 Jan 2006) was 3.4 X [10.sup.12] photons [cm.sup.-2] [s.sup.-1], calculated as photosynthetically active radiation (PAR) from irradiance at 1-m depth using an empirically determined attenuation coefficient (Biospherical Instruments PUV-541, cosine collector; [K.sub.PAR] = 0.498). Although photoreception is feasible for A. plebs under these shallow summer conditions, its visual capabilities during austral winter and at deeper depths of its range are not clear.
Both optical and physiological adaptations are commonly employed to increase photon capture for vision in dim light habitats (reviewed in Laughlin, 1990; Warrant and Locket, 2004). Optically, A. plebs has sacrificed spatial resolution to increase photon capture by having relatively few, large ommatidia (~260 ommatidia, 40-50 [micro]m wide; Meyer-Rochow and Tiang, 1979). Similar optical adaptations are seen in other lysianassid amphipods (Hallberg et al., 1980). Physiologically, its temporal resolution, as indicated by waveform dynamics of ERGs and maximum CFF, is quite low (Figs. 5, 6; Table 1). For comparison, Plesionika rossignoli, a pandalid shrimp living as deep as 1000 m, had the largest response latency (57.3 ms) and lowest maximum CFF (14.3 Hz), and therefore the slowest eye, from among 13 species of mesopelagic crustaceans studied at 5 [degrees]C by Frank (2003).
However, when comparing temporal resolution among different studies, one must consider the experimental temperatures and durations of the stimulus light flash because elevated temperature will decrease response latency and increase maximum CFF (Table 1), while longer stimulus flashes may slightly decrease response latency (T. Frank, unpubl. data). If a [Q.sub.10] of 2 is assumed for P. rossignoli, its response latency and maximum CFF at 3 [degrees]C (66 ms and 12.4 Hz) would still indicate a faster eye than that of dark-adapted A. plebs at the same temperature (122 ms, 11.67 Hz). Considering stimulus flash duration, the latency data from P. rossignoli (Frank, 2003) are in response to 100-ms flashes, whereas the latency data from A. plebs are calculated from 75-ms flashes. It is unlikely that this difference in flash duration is responsible for the magnitude of the latency difference between the two species (56 ms at 3 [degrees]C), as unpublished data from two species of caridean shrimp (Pasiphaea multidentata and Dichelopandalus leptocerus) demonstrated that differences between response latencies to stimulus flashes of 50 and 100 ms in the same animal are less than 3 ms (T. Frank, unpubl. data).
The spatial (optical) and temporal (physiological) adaptations of the A. plebs eye increase photon capture at the expense of resolving fine detail and capturing fast visual events (e.g., Warrant, 1999). As a benthic scavenger (Nyssen et al., 2005), A. plebs does not need to image fast-moving prey, and likely relies on chemoreception for locating carrion (Janecki and Rakusa-Suszczewski, 2004). Slow photoreceptors also require less energy (Laughlin et al., 1998), which fits with the opportunistic lifestyle of a scavenging amphipod. Maintaining visual sensitivity in low light conditions may aid in the avoidance of predators, such as notothenioid fishes (Foster et al., 1987; La Mesa et al., 2004).
Previous studies with A. plebs have shown that light adaptation at 0 [degrees]C and an increase in temperature to 10 [degrees]C in the dark cause similar migrations of screening pigment granules in retinular cells, but microvillar damage absent under light adaptation was severe in the dark at 10 [degrees]C (Meyer-Rochow and Tiang, 1979, 1982). We found that raising the experimental temperature from 3 to 7 [degrees]C had little effect on the irradiance sensitivity of A. plebs, but light adaptation reduced sensitivity (Fig. 4B, C). This suggests that at the environmentally unrealistic temperature of 7 [degrees]C, the A. plebs eye is still functional, and any screening pigment migration or microvillar damage that had occurred did not affect irradiance sensitivity.
The temporal resolution of A. plebs photoreceptors did not increase significantly with light adaptation (Table 1). After light adaptation, most arthropods have shortened photoreceptor response times due to changes in voltage-gatedion channel dynamics, resulting in increased photoreceptor speed (Wong, 1978; Weckstrom and Laughlin, 1995). Notable exceptions are slow-moving tipulid flies and most deep-sea crustaceans, which are thought to conserve energy by maintaining slow photoreceptor response dynamics when light adapted (Laughlin and Weckstrom, 1993; Frank, 2003). A. plebs appears to have a similar strategy, although intracellular methods are needed to fully characterize its membrane properties and compare them to well-studied fly models (e.g., Laughlin and Weckstrom, 1993).
In contrast to light adaptation, photoreceptor response dynamics did increase with temperature. The [Q.sub.10] for this effect (1.92) is similar to those reported for the change in temporal resolution with temperature in both flies (Tatler et al., 2000) and tunas (Fritsches et al., 2005). The experimental temperature increase likely accelerated the phototransduction cascade, as our [Q.sub.10] is near the range of 2-3 expected for biochemical reactions (Juusola and Hardie, 2001). Unlike some insects and predatory fish that are thought to improve temporal resolution through thermoregulation of their visual systems (e.g., Fritsches et al., 2005), A. plebs shows no indication of being capable of thermoregulation, and therefore should maintain the extremely slow photoreceptor temporal dynamics resulting from its stable, cold environment. Collectively, our electrophysiological data suggest that the A. plebs eye is adapted for a slow lifestyle in a low light environment, where maximizing photon capture occurs at the expense of detecting fast events in the visual scene.
We thank S. Dyhrman and R. Hannibal for help in the field, as well as D. Karentz and Raytheon Polar Services for arranging permits to transport specimens. This work was made possible by the U.S. National Science Foundation-sponsored International Graduate Training Course in Antarctic Biology (NSF grant # OPP-05-04072 to D. Manahan), and light data presented here were collected by the course. Additional funding was provided by a postdoctoral fellowship to J.H.C. from the Harbor Branch Oceanographic Institution, and by NSF grant #IBN-0343871 to T.M.F. This is Harbor Branch contribution #1635.
Arntz, W. E., T. Brey, and V. A. Gallardo. 1994. Antarctic zoobenthos. Oceanogr. Mar. Biol. Annu. Rev. 32: 241-304.
Arrigo, K. R., D. H. Robinson, and C. W. Sullivan. 1993. A high resolution study of the platelet ice ecosystem in McMurdo Sound, Antarctica: photosynthetic and bio-optical characteristics of a dense microalgal bloom. Mar. Ecol. Prog. Ser. 98: 173-185.
Barth, F. G., T. Nakagawa, and E. Eguchi. 1993. Vision in the ctenid spider Cupiennius salei: spectral range and absolute sensitivity. J. Exp. Biol. 181: 63-79.
Donner, K. O. 1971. On vision in Pontoporeia affinis and P. femorata (Crustacea, Amphipoda). Commentat. Biol. 41: 3-17.
Foster, B. A., J. M. Cargill, and J.C. Montgomery. 1987. Planktivory in Pagothenia borchgrevinki (Pisces: Nototheniidae) in McMurdo Sound, Antarctica. Polar Biol. 8: 49-54.
Frank, T. M. 1999. Comparative study of temporal resolution in the visual systems of mesopelagic crustaceans. Biol. Bull. 196: 137-144.
Frank, T. M. 2003. Effects of light adaptation on the temporal resolution of deep-sea crustaceans. Integr. Comp. Biol. 43: 559-570.
Frank, T. M., and J. F. Case. 1988. Visual spectral sensitivities of bioluminescent deep-sea crustaceans. Biol. Bull. 175: 261-273.
Frank, T. M., and E. A. Widder. 1999. Comparative study of spectral sensitivities of mesopelagic crustaceans. J. Comp. Phyisol. A 185: 255-265.
Fritsches, K. A., R. W. Brill, and E. J. Warrant. 2005. Warm eyes provide superior vision in swordfishes. Curr. Biol. 15: 55-58.
Glantz, R. M. 1968. Light adaptation in the photoreceptors of the crayfish, Procambarus clarki. Vision Res. 8: 1407-1421.
Govardovskii, V. I., N. Fyhrquist, T. Reuter, D. G. Kuzmin, and K. Donner. 2000. In search of the visual pigment template. Vis. Neurosci. 17: 509-528.
Hallberg, E., H. L. Nilsson, and R. Elofsson. 1980. Classification of amphipod compound eyes: the fine structure of the ommatidial units (Crustacea, Amphipoda). Zoomorphologie 103: 59-66.
Hamdorf, K., P. Hochstrate, G. Hoglund, M. Moser, S. Sperber, and P. Schlecht. 1992. Ultra-violet sensitizing pigment in blowfly photoreceptors R1-6: probable nature and binding sites. J. Comp. Physiol. A 171: 601-615.
Isla, E., D. Gerdes, A. Palanques, N. Teixido, W. Arntz, and P. Puig. 2006. Relationships between Antarctic coastal and deep-sea particle fluxes: implications for the deep-sea benthos. Polar Biol. 29: 249-256.
Janecki, T., and S. Rakusa-Suszczewski. 2004. The effect of glutamic acid (glu) and kynurenic acid (kyn) on the metabolism of the Antarctic amphipod Abyssorchomene plebs. J. Crustac. Biol. 24: 81-83.
Johnson, M. L., E. Gaten, and P. M. J. Shelton. 2002. Spectral sensitivities of five marine decapod crustaceans and a review of spectral sensitivity variation in relation to habitat. J. Mar. Biol. Assoc. UK 82: 835-842.
Juusola, M., and R. C. Hardie. 2001. Light adaptation in Drosophila photoreceptors. II. Rising temperature increases the bandwidth of reliable signaling. J. Gen. Physiol. 117: 27-41.
La Mesa, M., M. Dalu, and M. Vacchi. 2004. Trophic ecology of the emerald notothen Trematomus bernacchii (Pisces, Nototheniidae) from Terra Nova Bay, Ross Sea, Antarctica. Polar Biol. 27: 721-728.
Lall, A. B., and T. W. Cronin. 1987. Spectral sensitivity of the compound eyes in the purple land crab Gecarcinus lateralis (Freminville). Biol. Bull. 173: 398-406.
Land, M., and D.-E. Nilsson. 2002. Animal Eyes. Oxford University Press, Oxford.
Laughlin, S. B. 1990. Invertebrate vision at low luminances. Pp. 223-250 in Night Vision, R. F. Hess, L. T. Sharpe, and K. Nordby, eds. Cambridge University Press, Cambridge.
Laughlin, S. B., and R. C. Hardie. 1978. Common strategies for light adaptation in the peripheral visual systems of fly and dragonfly. J. Comp. Physiol. 128: 319-340.
Laughlin, S. B., and M. Weckstrom. 1993. Fast and slow photoreceptors--a comparative study of the functional diversity of coding and conductances in the Diptera. J. Comp. Physiol. A 172: 593-609.
Laughlin, S. B., R. R. de R. van Steveninck, and J. C. Anderson. 1998. The metabolic cost of neural information. Nat. Neurosci. 1: 36-41.
Lythgoe, J. N. 1979. The Ecology of Vision. Clarendon Press. Oxford.
Marshall, N. J., T. W. Cronin, and T. M. Frank. 2003. Visual adaptation in crustaceans: chromatic, developmental, and temporal aspects. Pp. 343-372 in Sensory Processing in Aquatic Environments. S. P. Collin and N. J. Marshall, eds. Springer-Verlag, New York.
Maykut, G. A., and T. C. Grenfell. 1975. The spectral distribution of light beneath first-year sea ice in the Arctic Ocean. Limnol. Oceanogr. 20: 554-563.
Meyer-Rochow, V. B. 1980. Eye colour and spectral sensitivity in the Antarctic amphipod Orchomene plebs. N. Z. Antarctic Record 3: 25-28.
Meyer-Rochow, V. B., and K. M. Tiang. 1979. The effects of light and temperature on the structural organization of the eye of the Antarctic amphipod Orchomene plebs (Crustacea). Proc. R. Soc. Lond. B 206: 353-368.
Meyer-Rochow, V. B., and K. M. Tiang. 1982. Comparison between temperature-induced changes and effects caused by dark/light adaptation in the eyes of two species of Antarctic crustaceans. Cell Tissue Res. 221: 625-632.
Minke, B., and K. Kirschfeld. 1979. The contribution of a sensitizing pigment to the photosensitivity spectra of fly rhodopsin and metarhodopsin. J. Gen. Physiol. 73: 517-540.
Naka, K. I., and W. A. H. Rushton. 1966a. S-potentials from colour units in the retina of fish (Cyprinidae). J. Physiol. 185: 536-555.
Naka, K. I., and W. A. H. Rushton. 1966a. S-potentials from luminosity units in the retina of fish (Cyprinidae). J. Physiol. 185: 587-599.
Nyssen, F., T. Brey, P. Dauby, and M. Graeve. 2005. Trophic position of Antarctic amphipods--enhanced analysis by a 2-dimensional biomarker assay. Mar. Ecol. Prog. Ser. 300: 135-145.
Rakusa-Suszczewski, S. 1982. The biology and metabolism of Orchomene plebs (Hurley 1965) (Amphipoda: Gammaridae) from McMurdo Sound, Ross Sea, Antarctica. Polar Biol. 1: 46-54.
Robinson, D. H., K. R. Arrigo, R. Iturriaga, and C. W. Sullivan. 1995. Microalgal light-harvesting in extreme low-light environments in McMurdo Sound, Antarctica. J. Phycol. 31: 508-520.
Stavenga, D. G., R. P. Smits, and B. J. Hoenders. 1993. Simple exponential functions describing the absorbance bands of visual pigment spectra. Vision Res. 33: 1011-1017.
Tatler, B., D. C. O'Carroll, and S. B. Laughlin. 2000. Temperature and the temporal resolving power of fly photoreceptors. J. Comp. Physiol. A 186: 399-407.
Vetter, R. A. H., and F. Buchholz. 1998. Kinetics of enzymes in cold-stenothermal invertebrates. Pp. 190-211 in Cold Ocean Physiology, H. O. Portner and R. C. Playle, eds. Cambridge University Press, Cambridge.
Warrant, E. J. 1999. Seeing better at night: life style, eye design and the optimum strategy of spatial and temporal summation. Vision Res. 39: 1611-1630.
Warrant, E. J., and N. A. Locket. 2004. Vision in the deep sea. Biol. Rev. 79: 671-712.
Weckstrom, M., and S. B. Laughlin. 1995. Visual ecology and voltage-gated ion channels in insect photoreceptors. Trends Neurosci. 18: 17-21.
Wong, F. 1978. Nature of light induced conductance changes in ventral photoreceptors of Limulus. Nature 276: 76-79.
Zettler, F. 1969. Die Abhangigkeit des Ubertragungsverhaltens von Frequenz und Apatationszustand, Gemessen am einzelnen Lichtrezeptor von Calliphora erythrocephala. Z. Vgl. Physiol. 64: 432-449.
JONATHAN H. COHEN* AND TAMARA M. FRANK
Department of Visual Ecology, Division of Marine Science, Harbor Branch Oceanographic Institution, 5600 US 1 North, Fort Pierce, Florida 34946
Received 25 April 2006; accepted 11 July 2006.
* To whom correspondence should be addressed. E-mail: email@example.com
Abbreviations: CFF, critical flicker fusion frequency; ERG, electroretinogram; UV, ultraviolet.
Table 1 Temporal resolution of Abyssorchomene plebs photoreceptors Response latency (1) Time-to-peak (1) Treatment (ms) (ms) Dark-adapted, 3 [degrees]C 122 ([+ or -]6) 165 ([+ or -]1) Dark-adapted, 7 [degrees]C 83 ([+ or -]2) 138 ([+ or -]2) Blue-light-adapted, -- -- 3 [degrees]C Treatment Max CFF (2) (Hz) [Q.sub.10] (3) Dark-adapted, 3 [degrees]C 11.7 ([+ or -]0.33) 1.92 ([+ or -]0.32) Dark-adapted, 7 [degrees]C 15.0 ([+ or -]0.58) -- Blue-light-adapted, 14.0 ([+ or -]0.58) -- 3 [degrees]C Mean values are given with standard errors in parentheses. (1) n = 4 and 2, for 3 [degrees]C and 7 [degrees]C treatments, respectively. (2) n = 7, 3, and 5, for each treatment, respectively. (3) n = 3.
|Printer friendly Cite/link Email Feedback|
|Author:||Cohen, Jonathan H.; Frank, Tamara M.|
|Publication:||The Biological Bulletin|
|Date:||Oct 1, 2006|
|Previous Article:||Source and specificity of chemical cues mediating shelter preference of Caribbean spiny lobsters (Panulirus argus).|
|Next Article:||Caribbean placozoan phylogeography.|