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Crustacea) in the Northern Baltic Sea

Crustacea) in the Northern Baltic Sea

Journal of Experimental Marine Biology and Ecology L 246 (2000) 85±101 www.elsevier.nl/locate/jembe

Eye function of (Crustacea) in the northern

Magnus LindstromÈ * TvarminneÈ Zoological Station, University of Helsinki, FIN-10900 Hanko, Received 5 August 1999; received in revised form 20 October 1999; accepted 28 November 1999

Abstract

Eye spectral sensitivity, [S(l)], was measured in seven northern Baltic mysid using an electroretinogram technique. Their S(l) curves were compared with the spectral distribution of underwater light at their normal habitats. In the littoral species ,

¯exuosus and Praunus inermis, the S(l) maxima, [S(l)max ], were in the wavelength-bands of 525±535, 505±515 and 520±530 nm respectively. The neoimmigrant species Hemimysis anomala had a S(l)max around 500 nm and high sensitivity at 393 nm, possibly indicating UV-sensitivity. S(l) of the pelagic species mixta and Mysis relicta sp. II was at about 505±520 nm. M. relicta sp. I from Pojoviken Bay and fresh water humic Lake PaajarviÈÈ È had S(l)atmax ¯ 550 nm and 570 nm respectively. This is in accordance with a similar long-wavelength shift in light transmittance of the respective waters. The eyes of the latter population were also damaged by strong light. The pontocaspian neoimmigrant H. anomala is clearly adapted to waters transmitting more blue light.  2000 Elsevier Science B.V. All rights reserved.

Keywords: Adaptation to UWL; Baltic Sea; ERG; Mysidacea; Light damage; Spectral sensitivity

1. Introduction

Traditionally ®ve mysid species have been attributed to the northern Baltic Sea, namely the pelagic glacial relict species Mysis relicta Loven, the pelagic Mysis mixta Lilljeborg, the benthic opportunist Neomysis integer (Leach), and the phytal species Praunus ¯exuosus (Muller)È and Praunus inermis (Rathke) (Segerstrale,Ê 1945; JarvekulgÈÈ and Veldre, 1963; Salemaa et al. 1986).VainolaÈÈÈ (1986) however split M. relicta into two separate species, M. relicta I and M. relicta II, on the basis of electrophoretic ®ndings. A

*Tel.: 1358-19-280-148; fax: 1358-19-280-122. E-mail address: magnus.lindstrom@helsinki.® (M. Lindstrom)È

0022-0981/00/$ ± see front matter  2000 Elsevier Science B.V. All rights reserved. PII: S0022-0981(99)00178-1 86 M. LindstromÈ / J. Exp. Mar. Biol. Ecol. 246 (2000) 85 ±101 few years later the pontocaspian sublittoral immigrant Hemimysis anomala was ®rst found by Salemaa and Hietalahti (1993). The mysids have an important role as predators and prey in the Baltic ecosystem (Gorokhova and Hansson, 1997; Viitasalo and Rautio, 1998) as well as in other seas (Mauchline, 1980, 1982). Their schooling behaviour and choice of speci®c habitats, their diurnal migrations and feeding behaviour point to extensive use of vision. M. relicta has been shown to use vision in prey catching (Ramcharan and Sprules, 1986). Also the big eyes with hundreds of ommatidia indicate the importance of light and light ¯uctuations in their lives. M. mixta, however, feeds more ef®ciently in darkness (Rudstam et al., 1989) but obviously also uses vision in low light conditions (own observations). The prerequisite for vision is that the visual pigment of an eye is able to absorb radiation within the spectrum of available light. The light spectrum becomes narrower with depth [Tyler, 1959, colour picture in Levine and MacNichol (1982)]. The narrower the spectrum and the lower the light intensity, the more important it is for the that the eye visual pigment absorbs as much as possible of the available light. This implicates tuning of the pigment's absorption maximum towards the wavelengths of maximal light transmission. This concept may also be applied to mysids, inhabiting a wide range of habitats in the Baltic sea and in lakes with waters of different spectral properties. Relatively few measurements have been conducted on mysid spectral sensitivity [S(l)]. Beeton (1959) used the activity spectrum of M. relicta to calculate its S(l), and so did Herman (1962) with Neomysis americana. S(l) and light tolerance of M. relicta were investigated by LindstromÈ and Nilsson (1984, 1988), S(l)ofN. integer, P. ¯exuosus and M. mixta by LindstromÈ (1992) and light damage in M. relicta caused by excessive light by LindstromÈÈ et al. (1988), and Meyer-Rochow and Lindstrom (1997). Spectrophotometric measurements of the M. relicta visual pigment has been performed by Gal et al. (1999) and of visual and screening pigments by Dontsov et al. (1999). An adaptation of the visual system to the photic environment has been demonstrated in ®sh by comparing the absorbance spectrum of visual pigments in solution with the available light spectrum (Munz and McFarland, 1973; Levine and MacNichol, 1982). The absorbance maximum of the pigment is frequently shifted to shorter wavelengths for species living in oceanic waters, with maximum transmittance in the blue, whereas the pigments of species living in fresh waters, with maximum transmittance in the red, usually have absorbance maxima at longer wavelengths (Lythgoe, 1972, 1979), although Govardovskii (1976) doubted the signi®cance of this sensitivity hypothesis for ®shes. without colour vision have only one visual pigment. The S(l) of the eye is not always exactly the same as the absorbance spectrum of the visual pigment. Different structures in the eye may alter the light spectrum reaching the rhabdom (Goldsmith, 1978). In crabs Forward et al. (1988) also rejected the sensitivity hypothesis, basing their opinion on microspectrophotometrically measured visual pigment spectra from 27 species of crabs. Donner (1971), however, showed an almost perfect correspondence between S(l) maxima [S(l)max ] of the amphipod Monoporeia [Pontoporeia] af®nis as well as Pontoporeia femorata and the spectral distribution of light in the Baltic Sea. In the isopods Cirolana borealis and Saduria entomon, LindstromÈ and Nilsson (1983) and

LindstromÈ et al. (1991) found good correspondence between S(l)max and spectral distribution of underwater light (UWL) in the animals' habitats in the North Sea and the Baltic Sea, respectively. M. LindstromÈ / J. Exp. Mar. Biol. Ecol. 246 (2000) 85 ±101 87

During the last years there has been extensive research on mysid ecology in the northern Baltic Sea (Rudstam and Hansson, 1990; Salemaa et al., 1990; Kauppila, 1994; Nordstrom,È 1997; Viherluoto, 1998; Viitasalo and Rautio, 1998; Gorokhova, 1999). This called for a review on what is known about mysid vision in this area, with the two species of M. relicta separated, and the newcomer of the nineties, the pontocaspian neoimmigrant H. anomala included. The aim of this review is to show to what extent the eyes of mysids from the Finnish coastal area are adapted to the light conditions prevailing in their normal habitats. The S(l) recorded from the eyes of the different species are compared with the spectrum of downwelling light in their respective habitats.

2. Material and methods

2.1. The species

2.1.1. M. mixta and M. relicta M. mixta dominates over the two partially sympatric sibling species of M. relicta (sp. I and sp. II, Vainola,ÈÈÈ 1986; Vainola ÈÈÈ and Vainio, 1998) in the western parts of the Gulf of Finland and in the northern Baltic proper (Salemaa et al., 1986). In the Bothnian Sea the M. mixta and the M. relicta group species occur in about equal numbers. M. relicta is the more euryhaline of the two, and tolerates the lower salinity waters of the Bothnian Bay. All species require benthic contact (Salemaa et al., 1990) and are oxygen- demanding, thus avoiding anoxic bottoms. Both feed on phyto- and ; M. mixta mainly on zooplankton (Rudstam, 1988; Viherluoto, 1998). One generation is produced annually. In all three species, most of the population undertakes nocturnal vertical migrations, part remaining close to the bottom also at night. M. mixta avoids light levels exceeding 1024 lux (estimated value, Rudstam et al., 1989; Rudstam and Hansson, 1990). M. relicta is also found in many Finnish lakes, where it also undertakes nocturnal vertical migrations during the summer months (Hakala, 1978). Samples of populations conventionally identi®ed as M. relicta were collected from two Baltic Sea localities using a bottom sledge ending in a plastic bag. From the deep (max. 86 m), dark-water humic lake, Lake PaajarviÈÈ È the animals were collected with a vertically towed net from about 60 m. The Baltic material was later found to include two species, inseparable by anatomical means, provisionally named sp. I and sp. II (Vainola,ÈÈÈ 1986; VainolaÈÈÈ and Vainio, 1998). After collection the animals were stored in darkness at the temperature prevailing at the sampling locality. The Baltic material was collected in 1972 (Lindstrom,È 1976) and 1991 from TvarminneÈÈ Storfjard in the outer archipelago near Tvarminne È Zoological Station. The 1991 sample was electrophoretically identi®ed as sp. II of the M. relicta group (R. Vainola,ÈÈÈ pers. commun.). Samples of the population from the Pojoviken Bay (a fjord in the Gulf of Finland) were collected in 1983 and 1985, and the population in Lake PaajarviÈÈ È in 1982, 1983 and 1987 (Lindstrom È and Nilsson, 1984, 1988). These two populations belong to the M. relicta group sp. I (Vainola,ÈÈÈ 1986). 88 M. LindstromÈ / J. Exp. Mar. Biol. Ecol. 246 (2000) 85 ±101

2.1.2. N. integer, P. ¯exuosus and P. inermis N. integer and P. ¯exuosus were collected by a hand-held net from the sheltered littoral zone in Tvarminne.È P. inermis was collected in the same way in an exposed sandy and rocky shore habitat. The animals were stored at the temperature prevailing at the sampling locality in darkness or at a low light light:dark cycle. N. integer is a genuinely brackish water species, which is common in the Baltic Sea (Segerstrale,Ê 1945). It occurs in great shoals in the sea grass meadows and occasionally pelagically further out at open sea. Adult individuals are found down to 40 m in late summer. It is omnivorous, but prefers to feed on zooplankton (Rudstam et al., 1986; Uitto et al., 1995). It has two generations a year. The species is a large component of ®sh diets (Mauchline, 1980). P. ¯exuosus occurs in small shoals among , in inshore habitats, and so does P. inermis, which, however, does not shoal.

2.1.3. H. anomala In 1992, H. anomala was seen for the ®rst time in the Baltic Sea by a diver in the South-West archipelago of Finland (Salemaa and Hietalahti, 1993). It occurs in swarms at depths of 2±12 m in rocky crevices and in cavities of boulder shores but from 1996 has been found several times in shallow water close to the shore. H. anomala was collected by divers in 1993. The animals were stored in darkness at the temperature prevailing at the sampling site.

2.2. Electroretinogram (ERG) technique

S(l) and light tolerance of the eye was measured using the ERG technique. Only the main features will be dealt with here as the method is described elsewhere (Donner, 1971; LindstromÈÈÈ and Nilsson, 1983, 1988; Nilsson and Lindstrom, 1983; Lindstrom et al., 1988). A hole was punched through the corneal cuticle of one eye with a microneedle. Since the eyes contain between 600 and 2000 ommatidia, only a few are destroyed by the procedure. The electrode, a glass micropipette ®lled with a saline solution (1 M NaCl) and with a tip diameter of about 10 mm, was lowered about 50 mm into the eye. The neutral electrode was a Ag(AgCl) wire in contact with the Ringer solution (brackish water). After it had become evident that the eyes of the lake mysid were easily damaged by strong light (LindstromÈ and Nilsson, 1984), the animals were collected at night and the preparations were performed in infrared (IR) light, using IR image converters (LindstromÈ and Nilsson, 1983, 1988). Recordings performed earlier (M. relicta sp. II, N. integer and M. mixta) were repeated using the IR technique. Always the same dorsal region of the eye was aimed for when the electrode was inserted (Fig. 2 in LindstromÈ and Nilsson, 1988). The preparations were left to adapt for 1±2 h before the experiments commenced. Storage time before preparation did not affect the results. Neither were there any differences between adults and juveniles. The eye was exposed to 600 ms light ¯ashes of 14 different wavelengths ranging from 406 to 673 nm in steps of ¯20 nm (Schott double-interference ®lters, half-band width 7±16 nm). In H. anomala and P. inermis also 393 nm was used. The responses were recorded on the oscilloscope. Calculation of the S(l) curves was based on the relative quantum intensities needed for each wavelength to evoke responses of equal amplitude M. LindstromÈ / J. Exp. Mar. Biol. Ecol. 246 (2000) 85 ±101 89 in the eye. Assuming the top of the S(l) curve to be symmetrical in shape in analogy with the absorption curves of rhodopsin in solution, I used the best ®t of Dartnall's nomogram to the blue and red ¯anks of the curve to determine the position of the

S(l)max . During the experiments, slow sensitivity changes sometimes occurred. These were corrected for by returning to the same wavelength about every 10 min. The resulting time-sensitivity curve was used for correcting all wavelengths to a ®xed moment of the experiment. The strange peak present in most curves at 549 nm is an artefact caused by a calibration error, later corrected.

2.3. Light measurements

The UWL spectra of the different water bodies were recorded at several occasions from 1984 on, independently of animal sampling using a QSM 2500 submersible quantum spectrometer (Techtum, Umea,Ê ) in quanta per m22 per second and nm (qu m22 s21 nm21 ). Also the integrated quantum ¯uxes from 400 to 750 nm were recorded (qu m22 s21 ). Measurements were performed at 1, 3, 5, 7, 10, 15, 20, 25 and 30 m depth or down to the limit of the meter's light detection. In the Baltic Sea the monitoring continued at irregular intervals for 12 months in 1989±1990. The UWL was measured around noon during moments of clear sky. The position of the spectral peak did not change at any of the three localities during the year, only the total amount of incident light. The spectra became increasingly narrower with depth, with unchanged wavelengths of maximum transmission. As the pelagial mysids spend the day close to the bottom, where it was too dark for the light meter even in daytime, I have chosen to present the spectral distributions of light at the different localities at depths at which the quantal ¯uxes were about equal.

3. Results and discussion

3.1. Light measurements

LindstromÈ and Nilsson (1988) reported the light spectra at 5 m depth to have maxima at about 555±575 nm in the open Baltic Sea, at 565±585 nm in the Pojoviken Bay and between 600 and 700 nm in Lake Paajarvi.ÈÈ È The light intensity, measured at a depth of 5 m, differed as much as one log unit between each of the three localities, the open sea having the highest and Lake PaajarviÈÈ È the lowest transparency. In the present in- vestigation the spectral transmission maxima have been stated more precisely at 565, 575 and 670 nm using data recorded from depths where the peaks are well discernible. It is notable that the spectra shown for about equal total quantal ¯ux (Fig. 1) are recorded at different depths, 20 m, 10 m and 5 m respectively. The Baltic Sea was classi®ed as water type coastal 3 by Jerlov (1976), with maximum transmission at 550 nm. However, at the sampling locality closer to the shore the light transmission of the water shifts to longer wavelengths because the water discharge from land contains humic substances. The Secchi depth changes considerably depending on 90 M. LindstromÈ / J. Exp. Mar. Biol. Ecol. 246 (2000) 85 ±101

Fig. 1. Spectral distribution of light at (A) 20 m depth (open circles), Baltic Sea; (B) 10 m (dots), Pojoviken Bay (Baltic Sea); and (C) 5 m (crosses), Lake Paajarvi.ÈÈ È the plankton situation, but may during favourable conditions reach 8 m (Feb. 1, 1996). The Pojoviken Bay is a bay of the Baltic Sea, separated from it by a shallow sill. It has still lower transparency, and the transmission maximum at longer wavelengths depend on discharge of humic substances from land and the SvartaÊ river, discharging at the end of the bay. Maximum Secchi depth was 5.25 m, and the colour value was 35±45 mg Pt l21 (Aug. 23, 1969, Niemi, 1973). The colour of the water of the mesohumic Lake Paajarvi,ÈÈ È maximum depth 86 m, varies between 40 and 60 mg Pt l21 (Ruuhijarvi, È 1974) and the Secchi depth between 1.8 and 2.4 m (Ilpo Hakala, pers. commun.).

3.2. S(l)

All the mysid species dealt with here responded to light stimuli by a corneal negative M. LindstromÈ / J. Exp. Mar. Biol. Ecol. 246 (2000) 85 ±101 91 on-response followed by a decay to baseline. The overall shape of the S(l) curves was somewhat broader than would have been expected from the nomograms by Dartnall (1953), constructed on the basis of visual pigments in solution. The shape of the curves resembled absorption curves for porphyropsin (Bridges, 1967). Porphyropsin was looked for by high performance liquid chromatography in the eye of M. relicta from Lake Paajarvi,ÈÈ È but was not found (Lindstrom È et al., 1988). A broad shape of the curve does not necessarily indicate presence of a second pigment in the eye. Eye structures may absorb light selectively, thereby depressing the peak of the curve. Even self-screening may occur to some extent (Goldsmith, 1978). Proximal screening pigment migration changes the S(l) of the Australian fresh water cray®sh (Cherax destructor)ona circadian scale (Bryceson, 1986). Probably N. integer, P. ¯exuosus, P. inermis, M. mixta and M. relicta sp. I and sp. II possess only one visual pigment, which rules out colour vision. For all species, the

S(l)max is at shorter wavelengths than the peak irradiance at the corresponding locality. Only H. anomala has a S(l) curve indicating a sensitivity increase at the far blue end of the spectrum. In future experiments it will be of great interest to extend the ERG recordings into the UV.

3.3. Pelagic mysids

The three different populations of M. relicta examined had different S(l) curves (Fig.

2). The animals captured in the open sea (sp. II) had a S(l)max between 505 nm (Lindstrom,È 1976) and 520 nm, the animals from Pojoviken Bay (sp. I) had their S(l)max at 550 nm, and the lake animals (sp. I) at 570 nm (LindstromÈ and Nilsson, 1984, 1988). The visual pigments of M. relicta sp. I were measured spectrophotometrically by Dontsov et al. (1999), who found minima of bleaching difference spectra at 550 and 580 nm for the sea and lake population respectively.

3.3.1. M. relicta sp. I.

In M. relicta sp. I, it was possible to compare the position of the S(l)max of two populations of the same species living in different water bodies, with different optical properties. The eyes of both populations responded to near-IR light (LindstromÈ and

Meyer-Rochow, 1987). The S(l)max at 570 nm in the lake population is among the most red-shifted spectral sensitivities known. The eye responded with relatively high signal amplitudes to IR light used for dark-adapted preparations of the isopod Cirolana borealis, for which the light was completely invisible (LindstromÈ and Nilsson, 1983). It is supposed that the two M. relicta sp. I populations became separated during the last glacial age about 9000 years ago when Lake PaajarviÈÈ È was formed (Ruuhijarvi, È

1974). Their S(l)max at 550 and 570 nm indicate a maybe still active evolutionary adaptation of the visual pigment towards the spectral peak of the downwelling light. The

S(l)max at 570 nm in M. relicta sp. I from Lake PaajarviÈÈ È has already almost reached the maximum wavelength of downwelling light in the Pojoviken Bay, 575 nm, which the bay population has not arrived at yet. This shows a plasticity of visual pigment evolution. The cause for the further and faster development of the S(l)max in the lake population might be found in stronger selection pressure, because of the much lower transparency of the lake water. The shift of the S(l)max towards longer wavelengths has 92 M. LindstromÈ / J. Exp. Mar. Biol. Ecol. 246 (2000) 85 ±101

Fig. 2. Relative spectral sensitivity of (A) M. relicta. sp. I from Lake PaajarviÈÈ È (N511); (B) sp. I from the Pojoviken Bay (Baltic Sea) (N511); (C) sp. II from the open sea (N53). In Figs. 2±4, curves are vertically displaced for clarity. increased the ability of the eye to absorb the weak reddish light prevailing in the lake. In deep water, a close match between the S(l)max and the light transmission maximum is of utmost importance for being able to see prey organisms, and to avoid predators (Lythgoe, 1968, 1972, 1979). The relatively great difference between the 570 nm pigment and the transmission maximum of 670 nm may depend on an inability of the pigment to develop further towards longer wavelengths. During summer days, the densest concentration of M. relicta in Lake PaajarviÈÈ È is found at about 15±30 m depth. During the night it migrates closer to the surface (Hakala, 1978; Gronholm,È 1980). It may be pointed out that in the lake the QSM quantum spectrometer was unable to record light deeper than about 7 m in daytime (LindstromÈ and Nilsson, 1988). The persistent M. LindstromÈ / J. Exp. Mar. Biol. Ecol. 246 (2000) 85 ±101 93 nocturnal vertical migration of sp. I thus indicates a high sensitivity of the eye, because the lower limit for light penetration determined by the 1% value is only 4 m for the wavelength band of maximum penetration, 600±700 nm (Elomaa, 1977), and the

S(l)max is at 570 nm. Factors which may affect the vertical distribution of the mysids are, except from high temperature and light, the presence of predating ®sh and the vertical migration of plankton prey organisms (Gronholm,È 1980).

3.3.2. M. relicta sp. II

The S(l)ofmax M. relicta sp. II at 505±520 nm, (Fig. 2) far from the spectral peak of light transmission, 565 nm, is in accordance with the results by Gal et al. (1999) who found only one single pigment with a S(l)max of 520 nm in M. relicta from Cayuga Lake, at a water peak transmission at 563 nm. Beeton (1959) recorded the activity spectrum of M. relicta and found a maximum at about 515 nm and shortening reaction times towards the near-UV end of the spectrum. He interpreted this as evidence that M. relicta would have two visual pigments. Neither in the present investigation, nor in the study by Gal et al. (1999), were there any indications of a second visual pigment in M. relicta. The latter authors discussed possible causes for Beeton's results. No direct comparisons with the Finnish mysids can, however, be drawn as the North American mysid belongs to M. relicta sp. IV (VainolaÈÈÈ et al., 1994).

3.3.3. M. mixta M. mixta is common in deeper water, further out from the shore where the water is clearer and more transparent. M. mixta is originally an Atlantic species later adapted to brackish water (Salemaa et al., 1986). In the North Atlantic, the maximum transmission is at about 500 nm (Jerlov, 1976). This may explain the displacement of the eye's

S(l)max (495±510 nm) from the maximum wavelengths of downwelling light in the Baltic Sea (Fig. 3). A displacement of the visual pigment's absorption maximum from the maximum wavelength of downwelling light will decrease the amount of light available for vision, and in vertical migration the preferred light intensities (if there are such) will consequently be found at different depths in water bodies of different light transmission properties. The situation may be comparable to the vertical zonation of the mysid Boreomysis megalops in experimental conditions after an exposure to strong light that caused pathological changes in the eye. Light exposed animals chose a position much closer to the surface during their nocturnal pelagic phase (Attramadal et al., 1985). A similar observation was made by Meyer-Rochow (1988) on blinded rock lobsters, Panulirus longipes. Both M. mixta and M. relicta are pelagic at night, and M. mixta is known to migrate closer to the surface than M. relicta sp. II (Salemaa et al., 1986). This ecological niche separation might be an effect of the slightly different visual capacities of the two species. The problem of comparing the visual sensitivities or action spectra of animals with different S(l)max in a spectrally de®ned environment is attacked by Gal et al. (1999), who for M. relicta introduced the unit ``mylux'' which is comparable to the human Lux concept, but is unique for every different S(l), and subsequently for every species or population too. 94 M. LindstromÈ / J. Exp. Mar. Biol. Ecol. 246 (2000) 85 ±101

Fig. 3. Relative spectral sensitivity of (A) Hemimysis anomala (N54); (B) Neomysis integer (N54); and (C) M. mixta (N56). In H. anomala the last wavelength used was 690 nm instead of 673 nm.

3.4. Littoral mysids

In shallow water the light spectrum is very broad and almost any position of the

S(l)max would be acceptable for maintaining high visual sensitivity. N. integer, P. ¯exuosus and P. inermis all had S(l)max making them well adapted to the available light in the phytal meadows where light of mostly longer wavelengths is absorbed by the chlorophyll of macroalgae and higher plants, shifting the transmitted spectrum towards shorter wavelengths. P. ¯exuosus had a S(l)max at 505±515 nm and P. inermis at 520±530 nm (Fig. 4). The opportunistic species N. integer, which is common pelagically as well as in the littoral, had S(l)max at 525±535 nm (Fig. 3). The S(l) max offset from the wavelengths of maximum irradiance may increase contrast sensitivity in all three M. LindstromÈ / J. Exp. Mar. Biol. Ecol. 246 (2000) 85 ±101 95

Fig. 4. Relative spectral sensitivity of (A) Praunus inermis (N54); and (B) Praunus ¯exuosus (N53). The peak at 549 nm, present in all curves in Figs. 1±3 is an artefact depending on a small calibration error, later corrected. species, according to the ``Contrast Hypothesis'' which assumes that in shallow water a receptor with maximum sensitivity offset from the maximum transmission of the UWL is the most ef®cient contrast detector (Lythgoe, 1968, 1972, 1979). All three species depend on zooplankton as food to a considerable extent, particularly P. ¯exuosus. Under certain circumstances P. ¯exuosus shows true prey selection (Viitasalo and Rautio, 1998) which emphasises their use of vision in .

3.5. The neoimmigrant H. anomala

H. anomala is a newcomer to the northern Baltic Sea. It was observed for the ®rst 96 M. LindstromÈ / J. Exp. Mar. Biol. Ecol. 246 (2000) 85 ±101 time in the late summer of 1992 (Salemaa and Hietalahti, 1993). The animal avoids direct light, and stays during the day in dense swarms under stones and in rocky crevices at a depth of 2±12 m. Thereby they resemble their Mediterranean relatives, Hemimysis speluncola and Hemimysis margale®, which both dwell in caves, the latter in a completely dark submarine cave (Alcaraz et al., 1986). The former species migrates daily to the exterior during the night for feeding (Riera et al., 1991; Coma et al., 1997).

The S(l)ofmax H. anomala is the most blue-shifted of any recorded in this investigation. The position of the maximum around 500 nm (Fig. 3) indicates that the species is adapted to a water body with light transmission properties different from that of the Baltic coastal water, which has a transmission maximum around 565 nm (Fig. 1). A decreased light detection at depths in the Baltic archipelago can be predicted by the fact that the eye of H. anomala at the wavelength of maximum transmission (¯565 nm) has a performance of only about 53%, compared to the wavelength of theoretical maximum performance, about 490 nm. H. anomala is found in the Caspian Sea and the Black Sea, from where it is supposed to have invaded the Baltic Sea through man-made waterways. Unfortunately no data are available for the light transmission spectrum in the Caspian or Black Seas. The sensitivity increase at the deep blue end of the spectrum may indicate the presence of a second, blue- or Ð maybe Ð UV-sensitive, pigment. The big sensitivity variation at 393 nm may indicate presence or low concentration of a second, blue-sensitive pigment, depending on the prehistory of the specimen. A rhodopsin visual pigment can become reisomerised by light absorbed by the photoproduct, the meta- rhodopsin (Donner et al., 1994). If the necessary light spectrum for the process is not available, the pigment concentration will be low until new pigment is formed. If H. anomala has got two pigments, it might possess colour vision. In this context it may be noted that the chromatophore pigments of H. anomala are red, which gives the animal a reddish appearance in contrast to the other species in which the chromatophore pigments are black. The sensitivity increase may also depend on a single pigment's small absorption increase towards the UV, as shown by Gal et al. (1999) for M. relicta in Cayuga Lake.

The position of the S(l)max at the blue end of the spectrum may give the species a small, temporal visual sensitivity advantage during precuspular hours. At sunset and sunrise the light spectrum of the top 2±3 m of the water column changes into a two-peak spectrum with a blue maximum at about 480±490 nm and another maximum in red, due to the Chappuis effect (Munz and McFarland, 1973; LindstromÈ and Nilsson, 1983).

4. Concluding remarks

4.1. Light tolerance and light damage

Crustaceans living in low light environments are frequently very light sensitive. Their eyes are often big, with large apertures, or ommatidial angles, as in the amphipod Monoporeia af®nis (Donner, 1971) and the isopod Cirolana borealis (Nilsson and Nilsson, 1981; LindstromÈ and Nilsson, 1983). Furthermore, there is no need for deep-living animals to shield their eyes from intense light. The very high sensitivity is M. LindstromÈ / J. Exp. Mar. Biol. Ecol. 246 (2000) 85 ±101 97 thus, in some species, combined with low light tolerance. Those species' rhabdoms are damaged by even moderate light intensities (Loew, 1976; Nilsson and Lindstrom,È 1983; LindstromÈÈ and Nilsson, 1984, 1988; Lindstrom et al., 1988). In the mysids the interommatidial angles are small, but the number of ommatidia is high. Screening pigments are present, which shield the eye from too intense light. In N. integer the screening pigments migrate quite slowly (Hallberg et al., 1980) but fast enough for an animal in the natural environment. It turned out that the eyes of M. relicta sp. I collected on a cloudy day in Lake PaajarviÈÈ È did not react to light stimuli until several days after the collection. They were practically blind, but within a week they recovered slowly, although not completely (LindstromÈ and Nilsson, 1984). Controlled series of experiments were performed to measure the light tolerance of their eyes (LindstromÈÈ and Nilsson, 1988; Lindstrom et al., 1988). After different times of exposure, changes in the ®ne structure of the rhabdoms were histologically examined. Even moderate light intensities during a short interval (1500 lux, 10 min¯29 mEm22 s21 with the lamp used; 1 mE equals 6.02 1027 quanta) depressed the eyes' sensitivity for several days. Stronger intensities enhanced the disruption of the microvillar membranes and signi®cantly decreased the amplitude of the ERG (LindstromÈ and Nilsson, 1988). A similar process had been found to occur in the scavenger isopod Cirolana borealis (Nilsson and Lindstrom,È 1983). There was no indication of any endogenous rhythm in the adaptational state of M. relicta's eye as has been shown to occur in many species (Larimer and Smith, 1980; NasselÈ and Waterman, 1980; Leggett and Stavenga, 1981; Horne and Renninger, 1988). Such a rhythm would make the eye much more vulnerable to light damage during the condition of dark adaptation. In N. integer light adaptation takes about 20 min (Hallberg et al., 1980). One can still not rule out the possibility that a slow increase in light intensity/slow lift of the collecting gear could have adapted the M. relicta eye through pigment migration into a more light tolerant state. A similar series of experiments was performed on the Pojoviken Bay population of M. relicta sp. I. In this population the functional recovery after light exposure was much faster (Meyer-Rochow and Lindstrom,È 1997). Temperature was shown to in¯uence the degree of damage and recovery in M. relicta sp. I from the lake exposed 1 h to 4000 lux (about 78 mE m22 s21 with the lamp used) at 48C and 148C (LindstromÈ et al., 1988). The results, supported by ERG and electron micrographs of the rhabdoms, led to the conclusion that the initial reconstitution of the visual pigment is faster at higher temperatures, but also that the breakdown of microvilli proceeds further at higher temperature. The animals' vertical migration is strongest during the period of warmer water, when they may migrate even through the thermocline. During normal conditions they do not migrate into light intensities strong enough to damage the microvilli. However, the temperature-enhanced increase of visual pigment reconstitution may serve in favour of keeping the light sensitivity on a high level. In M. relicta sp. I from the Pojoviken Bay similar temperature experiments, but with exposure 1 h at 60 000±80 000 lux (approximately 1200±1600 mEm22 s21 ), resulted in longer initial delay before the recovery commenced in the colder group (Meyer-Rochow and Lindstrom,È 1997). The sea population is more resistant to photo- 98 M. LindstromÈ / J. Exp. Mar. Biol. Ecol. 246 (2000) 85 ±101 induced accumulation of peroxidation products in the eye, because of the much higher amount of ommochrome screening pigment in the eye tissues (Dontsov et al., 1999). The lake population does not normally have any need to shield the eyes from strong light, hence the lack of light damage resistance. The animals migrate during night-time, and even at noon the light penetration into the water is so low that we were unable to detect any light at 10 m with the QSM 2500 (LindstromÈ and Nilsson, 1988). In the Pojoviken Bay, however, light has been detected as deep as at 20 m and in TvarminneÈ StorfjardÈ at 35 m. LindstromÈ (1990) discussed the possibility that capturing and releasing mysids in daytime could have caused light damage, and thereby low success when transplanting mysids from one lake to another to improve food stock for ®sh (Furst,È 1965, 1986). Damage has been shown to occur still 6 years after exposure to excessive light in the Norwegian lobster, Nephrops norvegicus (Loew, 1976; Shelton et al., 1985) in which also the dioptric apparatus is damaged (Gaten, 1988). Furthermore, for scientists working on the behaviour of , it should be stressed that vision of animals from dark environments may easily become impaired if collecting or handling takes place in strong light. There is now a strong concern that the around the hydrothermal vents in the deep-sea would have been permanently damaged by the lights of submersibles (Herring et al., 1999). That eyes are damaged by strong light is of course no universal rule. M. relicta sp. I from the sea was not damaged by light that blinded the lake population. The eye of the isopod Cirolana borealis was easily destroyed by light, but the isopod S. entomon, having about the same environmental requirements, could cope with strong light (LindstromÈ et al., 1991). The littoral mysid species thrive in strong light, and H. anomala has been easy to introduce into fresh water basins [for immigration history, see Salemaa and Hietalahti (1993)]. VainolaÈÈÈ (1986) showed that the mysid populations in the Pojoviken Bay and in Lake PaajarviÈÈ È are conspeci®c and genetically very similar, while the open sea mysids belong to another reproductively isolated and fairly recently diverged species. The results show that there may be functional intraspeci®c differences in the visual systems of mysids living in different photic environments like differences in S(l)max (Fig. 3A,B) and light tolerance. However, the interspeci®c differences in S(l)max between mysids living in relatively similar environments (Fig. 3B,C) are far greater, suggesting that phylogenetic constraints may ef®ciently retard the adaptation of the visual system on a time scale of thousands of years. A comparison of the different mysid groups' S(l)max with the spectral distribution of light in their habitats shows a strong relation, but also that the adaptation to the photic environment may still be in progress. There are numerous mysid-containing habitats in the Baltic Sea, as well as in lakes within the Baltic area, which differ in both spectral distribution and light transmission. From an evolutionary and ecological point of view it would be of great interest to know whether, or to what extent, the mysids of these environments differ in S(l) and light tolerance of the eye.

Acknowledgements

Thanks are due to the TvarminneÈ Zoological Station and to my teacher, the late Prof. M. LindstromÈ / J. Exp. Mar. Biol. Ecol. 246 (2000) 85 ±101 99

K.O. Donner. Financial support was given by the Walter and Andree de Nottbeck Foundation. Dr. Risto VainolaÈÈÈ explained the of the M. relicta group to me. Without his investigations the spectral sensitivity of Baltic M. relicta would still remain a mystery. Drs. V.B. Meyer-Rochow and H. Salemaa gave valuable comments on an early draft of the manuscript. [SS]

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