Behavioral responses to UVR

Behavioral responses to radiation often vary with wavelength. Some

Figure 3. Simultaneous images taken at (a) green (490-560 nm) and (b) ultraviolet (350-380 nm) wavelengths. Note the bright background in the UV image that silhouettes fish strongly, even against the reef. [Taken from Losey et al. 27.]

Figure 2. The ratio of UV-A (380 nm) to photosynthetically active radiation (PAR, 400-700 nm) in terms of W m~2. Data were collected during the summer of 2001 with a UV radiometer (model Biospherical GUV-521) located at the Lacawac Sanctuary in the Pocono Mts., PA, USA (41.23 N, 75.21 W). Sunrise (5.27 h) and sunset (20.37 h) for 17 June 2001 are denoted by the vertical dashed lines. Sunrise and sunset on 8 July 2001 occurred at 5.36 h and 20.37 h, respectively. During crepuscular periods, the UV:PAR ratio is higher because the light field is mostly composed of skylight (see Section 14.1). As the sun's elevation increases, the amount of PAR increases and the light field in dominated by solar radiation. Note that a similar increase in UV-A-to-PAR occurs when patches of clouds pass over the sun. This is shown between 17.0-19.0 h on 8 July 2001.

-17-Jun - 8-Jul wavelengths induce positive phototaxis or movement towards a light source while other wavelengths induce negative phototaxis or movement away from a light source. For many species, exposure to UVR (280-400 nm) and shorter-wavelength visible (i.e., blue light, 400-440 nm) light induces negative phototaxis. These negative phototactic or avoidance behaviors correspond to wavelengths that are also known to be potentially damaging or lethal [11,16]. In motile organisms, both vertical and horizontal movements have been observed in avoidance of exposure to damaging radiation [28-31], while in less motile organisms covering behaviors are exhibited [32]. Many organisms, such as sea anemones, sea urchins, and sea cucumbers, cover themselves with shells, rocks, and other materials during peak periods of irradiance. Hiding within burrows and among rocks and macrophyte beds, as seen in many amphibian and larval fish species, also helps organisms reduce exposure to damaging radiation.

14.3.1 Laboratory experiments

Thus far, behavioral responses to damaging light have primarily been examined in the laboratory using artificial UV radiation sources. Experiments have been conducted on a variety of organisms from both freshwater and marine systems occupying all trophic levels. At the lower trophic levels, both phytoplankton and protozoa have been shown to exhibit negative phototaxis to UVR. For example, individual cells within mats of the filamentous marine cyanobacteria Micro-coleus chthonoplastes were shown to migrate to greater depths in response to increased UV-B exposure [28]. The red-colored freshwater ciliate Blepharisma japonicum responded with backward swimming when exposed to wavelengths within the UV-B range but began swimming forward when exposed to visible light at 580 nm [33]. It is important to investigate the behavior of organisms at these lower trophic levels as their response to UVR may directly or indirectly influence responses of those at higher trophic levels.

Laboratory experiments have clearly demonstrated that the wavelength of incident radiation is an important behavioral cue for zooplankton. Certain freshwater cladocerans become more agitated and negatively phototactic in the presence of blue light but remain calm and positively phototactic to red light [29]. These "color dances" of Cladocera were hypothesized to cue zooplankton to high concentrations of algal food, which typically filters out short wavelengths greater than longer wavelengths (i.e., "red-dance" keeps individuals in place, "blue-dance" promotes wandering). However, it was also suggested that the patterns of the dances may explain patterns of diurnal vertical migration. More recent studies with monochromatic radiation have demonstrated that Daphnia magna are positively phototactic to visible light (421-600 nm) and negatively phototactic to UVR (260-380 nm) with maximal sensitivity at 340 nm [34], Copepods have also shown UV avoidance behavior in the laboratory. In small experimental enclosures examining horizontal movements, the freshwater cyclo-poid Cyclops serrulatus was found to avoid exposure to UV-B radiation (280-320 nm) [10]. This study also noted that UV behavioral responses correlated well with UV tolerance (i.e., UV-sensitive organisms avoid UV-B exposure, see Section 14.3.4). UVR avoidance behaviors were also detected in the marine echinoid larva Dendraster excentricus exposed to an artificial UV-visible radiation source (315-700 nm) [30].

Certain stream-dwelling organisms have been shown to be negatively phototactic to UVR in laboratory microcosm experiments. Macroinvertebrates that inhabit or feed on the tops or sides of rocks, such as larval stages of mayflies, caddisflies, and blackflies, exhibited increased drift to more shaded areas when exposed to increased UV-B radiation [31]. Drifting was 60-70% less in the UV-B shielded controls.

Interestingly, deep-sea crustaceans also respond behaviorally to UVR. Tethered individuals of the oplophorid shrimp Systellaspis debilis respond to changes in ambient UVR by pitching, changing swimming speed, and moving their feeding appendages [35]. Possible explanations for behavioral responses to UV in deep-sea crustaceans are discussed in Section 14.4.2.

For some organisms, short exposures to UVR inhibit movement altogether. For example, following exposure to artificial UV-B, veligers and post-veligers of the zebra mussel Dreissena polymorpha ceased all swimming and crawling motions. However, exposure to UV-A and visible light had no effect on behavior [36]. A similar delay in phototaxis was noted for the green algae Volvox aureus exposed to both artificial and solar UV-B radiation [37].

Although these studies provide valuable information regarding organismal responses to varying wavelengths of radiation (i.e., action spectra), they do not tell us how animals respond to natural levels of solar radiation. Artificial lamps generally do not exactly replicate the solar spectrum. UV-B lamps often have greater output in the UV-B range compared to the solar spectrum. In order to supplement UV-A and visible light, UV-A and cool white lamps are used in laboratory setups, and these lamps often have less output in the UV-A and visible range than solar radiation. The total intensity of these lamps in terms of energy or quanta may be similar to solar radiation, but the spectral composition varies greatly (i.e., skewed towards the shorter wavelengths). Solar simulators come the closest to replicating both the intensity and spectral output of the sun; however, these instruments are very expensive, only irradiate a small area, and are only used by a handful of laboratories.

14.3.2 Field experimen ts

Few field studies have examined behavioral responses of organisms to natural solar radiation. One of the difficulties in these studies is determining whether a behavior is in response to UVR or visible light. High UV systems are also high visible light systems, both of which are known to be potentially damaging [1,8,38]. In addition, many animals have a separate suite of responses to varying levels of visible light. Typically, experimental enclosures are constructed of materials that vary in UVR transmittance. Commonly used materials that transmit full solar radiation include polyethylene, quartz, and acrylic plastics such as OP-4 (CYRO Industries) and UVT (Spartech, Inc. formerly Tow-nsend/Glasflex), all of which can be expensive. UV-blocking materials include Mylar® D and acrylic plastics such as OP-2 (CYRO Industries) and Plexiglas®. While these materials vary in their UV transparency, they have similar transparencies in the visible range. Therefore, using a combination of these materials, behaviors and/or survival can be examined in the presence of full solar radiation, in the absence of UV-B radiation, and in the absence of UV-B and UV-A

radiation. It is important to note that these experiments do not provide information concerning responses to a single wavelength; instead, they examine the effect of removing particular wavebands (i.e., UV-B or UV-B and UV-A). Because they remove entire wavebands, the UV blocking materials also unavoidably change the total irradiance, which can confound results. However, the difference in total irradiance between the UV- transparent and UV-blocking materials is often less than 10%. Finally, except for quartz, which is extremely expensive and hard to fabricate, the usual UV-transparent materials tend to block a significant fraction (25-50%) of UV-B.

In the field, solar UV-B has been demonstrated to inhibit motility and oriented movement in phytoplankton such as eukaryotic flagellates, blue-green algae or cyanobacteria, and gliding green algae [39]. When motility is compromised, phytoplankton are at risk of being exposed to greater light intensities, which may result in a bleaching of pigments; or they may be exposed to reduced light intensities, which may result in a reduction in photosynthetic rates. Exposure to increased or decreased irradiances also depends on mixing processes as well as the buoyancy of the individual cells (see also Chapter 4).

Recent field studies have also reported that zooplankton exhibit UVR avoidance in nature. The first evidence of a vertical avoidance response of Daphnia to solar UVR was recently published [40]. In the presence of full solar radiation, D. pulicaria rapidly descended from the surface waters (1.5 m) of a high-UV lake. In the absence of UV-B and shorter wavelength UV-A radiation (<380 nm), the majority of D. pulicaria remained in the surface waters. Thus, a stronger negative phototactic response was detected in the presence of UVR than in the absence of UVR. Negative phototactic behaviors have also been observed in a population of D. catawba inhabiting a high-UV lake located in the Pocono Mts., PA, USA (Figure 4) [41]. Experiments conducted in this study demonstrated that, in some cases, D. catawba actually swim towards the surface waters in the absence of UVR in spite of the probable presence of fish kairomones (Figure 4). These field results for Daphnia are supported by smaller scale experiments conducted in the laboratory [42,43].

Although Daphnia often displayed a preference for the surface waters in the absence of UVR, the response was variable, with mean depths of Daphnia increasing in the absence of UVR [41]. The reason for this variability is unknown. One explanation is that irradiance differed among experiments. Although the experiments in this study were not designed to specifically test zooplankton responses to irradiance, preliminary observations suggest that as irradiance increased, Daphnia responded with increased negative phototaxis. Because the acrylic used to construct the UV-blocking columns did transmit some longer wavelength UV-A (50% transmittance at 384 nm), this may be an avoidance response to either longer wavelength UV-A light or visible light [40]. Other species, such as the freshwater copepod Diaptomus nevadensis, the marine copepod Acartia tonsa, the cladoceran Daphnia magna, and the hydromedusan Polyorchis penicillatus also become negatively phototactic in response to increasing irradiance, both in the UV and visible range [1,38].

The harpacticoid copepod Tigriopus californicus, which lives in shallow tide

Downward

Downward

Upward

% Individuals

Figure 4. A comparison of the downward and upward migrations of Daphnia catawba in the presence and absence of UVR. There were three UV-transparent columns and three UV-opaque columns. Each column was suspended 10 cm below the surface of Lake Giles, a high-UV lake located in northeastern PA, USA. The downward experiment was conducted on 14 July 2000 and the upward on 2 August 2000. Mean solar irradiance was measured with a LICOR model LI-200SA pyranometer near solar noon (1300 h) when the experiments were conducted. Mean solar irradiance equaled 659 Wm~2 on 14 July 2000 and 694 Wm~2 on 2 August 2000.

% Individuals

Figure 4. A comparison of the downward and upward migrations of Daphnia catawba in the presence and absence of UVR. There were three UV-transparent columns and three UV-opaque columns. Each column was suspended 10 cm below the surface of Lake Giles, a high-UV lake located in northeastern PA, USA. The downward experiment was conducted on 14 July 2000 and the upward on 2 August 2000. Mean solar irradiance was measured with a LICOR model LI-200SA pyranometer near solar noon (1300 h) when the experiments were conducted. Mean solar irradiance equaled 659 Wm~2 on 14 July 2000 and 694 Wm~2 on 2 August 2000.

pools, was found to aggregate in shaded regions of pools at midday but show no preference at dawn and dusk [44], These same authors used lab experiments to demonstrate that T. californicus responds more to UV-B than to visible radiation and suggest that they may possess UV photoreceptors.

Small stream invertebrates have also been noted to respond negatively to UVR in nature. Blackfly larvae appear to exhibit a diurnal emigration, or migration out of UV-exposed stream channels, during periods of peak irradiance but return to UV-exposed regions as irradiance levels decrease [45]. In streams that were experimentally shielded from UVR exposure, however, larvae remained in the stream channels throughout the day. Larvae were allowed to move freely between the treatments and on average larval densities in the UV-shielded channels were 161-168% greater than those in the UV-exposed channels.

Differences in the spawning depths of yellow perch, Perca flavescens, in a high-versus a low-UV lake suggest that yellow perch also avoid UV exposure. Spawning depth was reported to be deeper in a high-UV lake (median = 3.2 m) compared to a low-UV lake (median = 0.4 m) [46]. In addition, yellow perch eggs were incubated at the surface of each lake in a modified reciprocal transplant experiment. Eggs were exposed to full solar radiation, shielded from UV-B, or kept in the dark. In the high-UV lake, all eggs perished in all the light treatments, but survival time was longer (2-4 days) for eggs in the UV-B shielded treatment. Furthermore, those collected from the high-UV lake survived longer than those collected from the low-UV lake. Most eggs (>96%) incubated in the light treatments of the low UV lake as well as the dark controls of both lakes survived to hatching. Comparable results, using a similar experimental design, were reported for the bluegill Lepomis machrochirus in which the median nesting depth was observed to be deeper in a high UV lake compared to a low UV lake [47].

It is more difficult to perform behavioral experiments in the open ocean. The approach has been to observe the distribution of organisms in relation to their photic environment combined with laboratory experiments examining UV tolerance and phototaxis. Both ascidians and sea urchins were shown to exhibit UV avoidance. The distribution of the solitary ascidian Corella inflata varied with exposure to direct solar radiation, particularly UVR exposure, with populations conspicuously absent from unshaded areas [48]. Laboratory experiments confirmed that UVR is lethal to all life history stages of C. inflata, with the younger stages being most vulnerable. In addition, none of the life stages possessed UV-absorbing photoprotective compounds. The sea urchins Arbacia punctulata and Lytechinus variegatus were shown to be negatively phototactic to bright solar radiation but positively phototactic to white light [49]. These data are consistent with the observation that echinoplutei migrate to deeper depths in the water column during peak periods of irradiance [30,50], but this response could also be related to other factors such as predator avoidance. The sea urchin Strongylocentrotus droebachiensis shades or covers itself in response to UVR exposure, particularly in response to UV-B or a combination of UV-B and UV-A [32]. Covering behavior was also shown to increase with increasing intensity of UVR exposure. In some sea urchin species, covering behavior has been observed to vary diurnally, with the greatest response during peak irradiance [49,51].

14.3.3 Relation to UV tolerance, pigmentation, andphotorepair

Behavioral responses to UVR appear to be related to UV tolerance (i.e., defined as the sum of an organism's photoprotection (pigmentation) and photorepair capabilities). For example, during periods of high UV, organisms occupying the surface waters of Lake Giles, a high UV lake in the Pocono Mts., PA, USA, were found to be more UV-tolerant than those inhabiting deeper waters during the day [12]. Laboratory experiments with the ostracod Cypris sp. demonstrated that this species is highly tolerant to UV-B exposure and actually showed a behavioral preference or positive phototaxis towards UV-B irradiance [10]. In the same study, the protozoan Paramecium aurelia was also shown to be highly tolerant and positively phototactic to UV-B irradiance [10].

The action spectrum of phototaxis in copepods has been demonstrated to depend on pigmentation. Within the visible light spectrum, Diaptomis nevadensis swimming speeds were faster in blue light compared to red light [38]. In addition, less pigmented individuals were more responsive to changes in wavelength than pigmented individuals [52]. Similar results have been reported for melanized Daphnia within the UV spectrum [43].

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