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Danio Rerio</Italic> Larvae: Observations F © 2020. Published by The Company of Biologists Ltd | Biology Open (2020) 9, bio047779. doi:10.1242/bio.047779 RESEARCH ARTICLE The effects of temperature on the proxies of visual detection of Danio rerio larvae: observations from the optic tectum Ewa Babkiewicz1,*, Michał Bazała2, Paulina Urban3,4, Piotr Maszczyk1, Magdalena Markowska5 and Z. Maciej Gliwicz1 ABSTRACT INTRODUCTION Numerous studies have indicated that temperature improves the Since temperature affects metabolic (Gilloly et al., 2001) and visual capabilities of different ectotherms, including a variety of fish behavioural (e.g. Chen et al., 2003) as well as almost all other species. However, none of these studies has directly tested whether biological rates (Brown et al., 2004), it strongly affects the fitness of elevated temperature extends the visual detection distance – the ectotherms. The literature provides numerous examples of studies distance from which a visual stimulus is detected. To test this indicating that temperature affects a variety of physiological hypothesis, we investigated the effect of temperature on the visual performances, including the functioning of visual capabilities in detection distance of zebrafish (Danio rerio) larvae by measuring the terrestrial and aquatic ectotherms. The evidence comes from three largest distance from a moving target that induced a neural response groups of studies. in the optic tectum. We applied advanced methods of functional The first group of studies described the observation that several calcium imaging such as selective plane illumination microscopy in large marine predatory fishes, including several species of combination with a miniature OLED screen. The screen displayed an swordfishes (Carey, 1982; Fritsches et al., 2005), lamnid sharks artificial, mobile prey, appearing in the visual field of the larvae. We (Block and Finnerty, 1994), tunas (Dickson et al., 2000; Sepulveda performed experiments in three temperature treatments (18, 23 and et al., 2007) and mackerel (Gasterochisma melampus, Sepulveda 28°C) on transgenic fish expressing a fluorescent probe (GCaMP5G) et al., 2007) independently evolved the mechanisms of partial that changes intensity in response to altered Ca2+ concentrations in cranial endothermy, or even whole-body endothermy, as in the case the nerves in the optic tectum. Based on the obtained data, we also of opah (Lampris guttatus, Wegner et al., 2015). Opah produces measured three additional parameters of the neural response in heat through the constant movement of its pectoral fins and the optic tectum, each being a proxy of sensitivity to changes in the minimises heat loss through a series of counter-current heat stimulus movement. We did not confirm our hypothesis, since exchangers within its gills (Wegner et al., 2015). In the case of the visual detection distance shortened as the temperature partial endothermy, as, for example, in the generally ectothermic increased. Moreover, all of the three additional parameters tunas (family Scombridae), cranial counter-current heat indicated a negative effect of the temperature on the speed of the exchangers, retia mirabilia, conserve metabolic heat, allowing neural response to the stimuli. However, the obtained results could be cranial temperatures to be elevated above the ambient water explained not only by worse visual capabilities at the elevated temperature (Holtz, 2013). These abilities allow elevated eye and temperature, but also by the differences in the visual field and in turn, brain temperatures to be maintained (Block, 1986; Sepulveda et al., the retinotopic location of the visual stimulus between the temperature 2007; Fritsches et al., 2005; Runcie et al., 2009). Despite their high treatments, since the stimulus in the experiments moved horizontally energy costs, these phenomena are treated as an adaptation rather than forward and backward from the fish’seye. improving the ability to detect and in turn to hunt prey more efficiently while diving in deep and cold marine water layers (Block and Finnerty, 1994). In the case of swordfishes, partial cranial KEY WORDS: Detection distance, Reaction distance, Perception, Zebrafish, Temperature, Visual stimuli endothermy helps to prevent the rapid deterioration of temporal resolution with decreasing temperature when the swordfish descends to deeper and cooler water layers (Fritsches et al., 2005). 1Department of Hydrobiology, Faculty of Biology, University of Warsaw at Biological The whole-body endothermy of opah allows for enhanced temporal and Chemical Research Centre, Żwirki i Wigury 101, 02-089 Warsaw, Poland. resolution and neural conductance of the eye and brain (Wegner 2Laboratory of Neurodegeneration, International Institute of Molecular and Cell et al., 2015). Biology in Warsaw, Księcia Trojdena 4, 02-109 Warsaw, Poland. 3Laboratory of Functional and Structural Genomics, Centre of New Technologies, University of The second group of studies assessed the effect of temperature on Warsaw, Banacha 2c, 02-097 Warsaw, Poland. 4College of Inter-Faculty Individual the activity of photoreceptors in the retina, mainly of insects and Studies in Mathematics and Natural Sciences, University of Warsaw, Banacha 2c, 02-097 Warsaw, Poland. 5Department of Animal Physiology, Faculty of Biology, fishes in response to light stimuli, most often using the University of Warsaw, Miecznikowa 1, 02-096 Warsaw, Poland. electroretinography method. Some of these studies tested the effect of temperature on the spectral sensitivity of retinal *Author for correspondence ([email protected], [email protected]) photoreceptors to different wavelengths of light in the visible range. For instance, Saszik and Bilotta (1999) performed E.B., 0000-0003-2398-8448; P.U., 0000-0001-6469-8776; P.M., 0000-0002- experiments in the same intensity and frequency, but with 1738-419X different spectral compositions of light to assess the spectral This is an Open Access article distributed under the terms of the Creative Commons Attribution sensitivity of adult zebrafish (Danio rerio) reared in darkness and in License (https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed. different temperatures before the experiments. They revealed that individuals housed in the warmer temperature had greater sensitivity Received 9 September 2019; Accepted 2 June 2020 to longer wavelengths. In this way, they indirectly showed that the Biology Open 1 RESEARCH ARTICLE Biology Open (2020) 9, bio047779. doi:10.1242/bio.047779 retina of fish reared in warmer temperatures had a greater neurons (Ahrens et al., 2013), or possess an exogenous reporter (e.g. contribution of rhodopsin in relation to porphyropsin, since the Ashworth and Bolsover, 2002). latter photopigment absorbs longer wavelengths. The results are The advantages of using SPIM and transgenic fish larva provides consistent with previous studies (Bridges, 1964; Allen and the possibility to observe an intact organism that changes McFarland, 1973) that examined the rod pigment composition of fluorescence in response to alterations in the concentration of the golden shiner (Nofemigonus crysoleticas) during different Ca2+ in the neurons, allowing the assessment of the detection seasons and found that the amount of porphyropsin in fish caught distance from the visual stimuli on the almost complete visual during winter was greater than in individuals caught during pathway through the ocular nerves to the optic tectum. summer. Numerous studies also assessed the effect of temperature This study aimed to test the hypothesis that an elevated on the speed and accuracy of the response, measuring the retinal temperature extends the visual detection of visually-oriented response to light stimuli of the same spectral composition but at zebrafish larvae. The detection distance was assessed using the different illumination frequencies using temporal resolution as a SPIM method and defined as the largest distance from a moving measurement of the ability to handle different rates of change in target appearing in the fish’s visual field that induced a neural luminescence. These studies generally revealed that a higher response in the optic tectum. temperature increases the speed and improves the accuracy (precision) of the response, which would contribute to the RESULTS detection of smaller and/or faster moving objects (e.g. the prey or The oxygen concentration in the E3 medium measured before the the predator). This was shown, for instance, for the blowfly experiments outside the sample chamber of the Lightsheet Z.1 (Calliphora vicina; Tatler et al., 2000), the predatory owlfly microscope differed in different temperatures (10.6±0.2, 9.6±0.2 (Libelloides macaronius; Belušičet al., 2007), and a variety of fish and 8.4±0.2 mg l−1 for 18, 23 and 28°C, respectively). However, species, including European eel (Anguilla anguilla), Prussian carp the oxygen concentration in the chamber during the experiments (Carassius gibelio), spotted dogfish shark (Scyliorhinus canicula; was very similar in each of the temperature treatments (9.5±0.3). Gacič́et al., 2015), and swordfish (Xiphias gladius; Fritsches et al., The oxygen concentration inside the glass capillary filled with 2005). It was also revealed that temperature increases the frequency agarose and submerged in the E3 medium was only slightly lower of responses of the ocellar neurons in the retina to the third-order (±0.2–0.3 mg
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