Altered environmental light drives retinal change in the Atlantic Tarpon (Megalops atlanticus) over timescales relevant to marine environmental disturbance
© The Author(s) 2018
Received: 20 July 2017
Accepted: 9 January 2018
Published: 18 January 2018
For many fish species, retinal function changes between life history stages as part of an encoded developmental program. Retinal change is also known to exhibit plasticity because retinal form and function can be influenced by light exposure over the course of development. Aside from studies of gene expression, it remains largely unknown whether retinal plasticity can provide functional responses to short-term changes in environmental light quality. The aim of this study was to determine whether the structure and function of the fish retina can change in response to altered light intensity and spectrum—not over the course of a developmental regime, but over shorter time periods relevant to marine habitat disturbance.
The effects of light environment on sensitivity of the retina, as well as on cone photoreceptor distribution were examined in the Atlantic tarpon (Megalops atlanticus) on 2- and 4-month timescales. In a spectral experiment, juvenile M. atlanticus were placed in either ‘red’ or ‘blue’ light conditions (with near identical irradiance), and in an intensity experiment, juveniles were placed in either ‘bright’ or ‘dim’ light conditions (with near identical spectra). Analysis of the retina by electroretinography and anti-opsin immunofluorescence revealed that relative to fish held in the blue condition, those in the red condition exhibited longer-wavelength peak sensitivity and greater abundance of long-wavelength-sensitive (LWS) cone photoreceptors over time. Following pre-test dark adaption of the retina, fish held in the dim light required less irradiance to produce a standard retinal response than fish held in bright light, developing a greater sensitivity to white light over time.
The results show that structure and function of the M. atlanticus retina can rapidly adjust to changes in environmental light within a given developmental stage, and that such changes are dependent on light quality and the length of exposure. These findings suggest that the fish retina may be resilient to disturbances in environmental light, using retinal plasticity to compensate for changes in light quality over short timescales.
The ability of individual organisms to adapt to environmental change (i.e., phenotypic plasticity) supports fitness by allowing the colonization of new environments  and survival during environmental disturbance . These unanticipated changes to the physical environment require an organism to either evade environmental stressors or modify its physiology or behavior in order to survive. Aquatic habitats are particularly dynamic because factors including depth , suspended sediment , and dissolved organic matter can alter underwater light quality . These factors affect light intensity and spectrum, resulting in often predictable and characteristic differences in light quality among aquatic habitats . The dynamic nature of underwater light, along with the critical role of vision in survival may have driven the great diversity and plasticity of retinal form and function observed among fish species [5, 7, 8].
The life history of fish typically includes metamorphosis from a larval stage to one or more juvenile stages before reaching adult sexual maturity. Between these stages, many marine fish migrate to new light environments, which requires changes in visual function [9–16]. Retinal change is thought to occur in anticipation of or in concert with shifts in habitat [17–21], the outcomes of which can be strongly influenced by changes in light exposure over life history [e.g., 22].
Plasticity of retinal development in response to altered environmental light has been observed in a variety of species. Fish reared in atypical lighting conditions through the course of development exhibit differential retinal sensitivity between major life history stages [23–28]. Specifically, differences in rearing light intensity and spectrum affect the spectral sensitivity of photoreceptor cells , result in altered retinal architecture , and lead to changes in the expression of opsin proteins in the retina [22, 26–28]. However, the capacity of retinal plasticity to compensate for ‘unexpected’ or abrupt changes in underwater light quality within a given life history stage (that is, between major developmental transitions) remains largely unknown.
Major storms, eutrophication events, and other natural and anthropogenic disturbances occur over short timescales and can result in acute and often dramatic shifts in the intensity and spectrum of underwater light [29, 30]. These kinds of disturbances may have profound effects on the abilities of fish to feed, avoid predators, engage conspecifics, and ultimately survive. Several recent studies have shown that retinal gene expression can change in response to abrupt changes in light quality [31–33], in some instances occurring within days or hours of altered light onset [34, 35]. Aside from these studies of gene expression, however, the effects of light change on physiological sensitivity and architecture of the retina remain to be investigated over timescales relevant to environmental disturbance.
The Atlantic tarpon (Megalops atlanticus) is a marine fish species that has a long maturation period (∼ 7–10 year; ), that includes multiple distinct developmental transitions coupled with movement to new habitats with different light environments. In addition to robust developmental change , phenotypic plasticity of the retina would be particularly advantageous to this species because over its long-life span (> 55 years; ) M. atlanticus occupies and moves between inshore and near-shore waters, both of which are highly susceptible to the light-altering effects of coastal storms, eutrophication, and pollution.
In this study, juvenile M. atlanticus were used to investigate how the intensity and spectrum of environmental light affects the fish retina on 2- and 4-month timescales. Electroretinography (ERG) was used to determine the in vivo sensitivity of the M. atlanticus retina, allowing for the comparison of retinal function to lighting conditions. Anti-opsin immunofluorescence was used to examine the lengths and distributions of photoreceptors in the M. atlanticus retina, in an effort to identify the mechanisms underlying retinal sensitivity shifts. Determining the capacity of the M. atlanticus retina for light-induced phenotypic plasticity will indicate the resilience of fish vision to marine disturbances that result in acute changes in environmental light.
Specimen collection and maintenance
Specimens of Megalops atlanticus used in this study
19.4, 17.9, 18.4
19.8, 18.6, 19.2, 20.9
21.4, 17.9, 17.5, 18.4
20.7, 16.3, 16.5, 19.7
19.4, 22.0, 24.0, 24.4
23.3, 24.2, 22.9, 23.6
For the intensity experiment, eight M. atlanticus were placed in conditions of different light irradiance, but near-identical spectra (Fig. 1c, d). The light spectrum of each condition was engineered to approximate that of natural sunlight, and were provided by four 1.3 m-long, custom-made ‘Solar-Max’ LED light bars (BML Horticulture Inc., Austin, TX, USA). Preliminary analysis of M. atlanticus retinal sensitivity by electroretinography included differentiation of light activation of rod- and cone-based systems by analysis of a-wave and b-wave amplitudes [38, 39]. An abrupt change occured at ~ 3 μW s−1 cm−2 (Additional file 1: Figure S1). Thus, light intensities for the ‘bright’ and ‘dim’ light conditions were set at 2.5 mW and .325 μW s−1 cm−2, respectively, in order to activate cone-based and rod-based vision. Light intensities were measured and set using a radiant power meter with a silicon photodiode (Ophir Photonics, North Andover, MA). Changing the intensity of light bar output did not affect the light spectrum (measured with a Hyper OCR spectroradiometer, Satlantic LP, Halifax, Nova Scotia) between the two lighting conditions. After 60 days, the retinal sensitivity of the four M. atlanticus from each condition was tested in vivo by electroretinography, after which the fish were euthanized, eyes were removed, and eyecups prepared and fixed for immunofluorescence analyses (see below).
For fish in the spectral experiment, electroretinography (ERG) was used to determine spectral sensitivity of the retina. Fish were anesthetized with 75 mg L−1 tricaine methanesulfonate (MS-222) in seawater, transferred to a flow-through apparatus for perfusion of the gills, and dark-adapted for 45 min. A silver-wire recording electrode was placed on the cornea of one eye, a reference electrode was placed just posterior to that eye, and a ground electrode was placed in seawater adjacent to the body. Signals were amplified using an AM Systems (Carlsborg, WA, USA) differential microelectrode amplifier (gain: 1000x; bandpass 1 Hz-1 kHz), and digitized by an iWorx (Dover, NH, USA) amplifier before recording on a laptop using iWorx Labscribe Software. Stimulus light from a QTH lamp was passed through a grating monochromator, an electronic fast-acting shutter (Uniblitz, Rochester, NY) and a 60 cm liquid light guide (Oriel Instruments, Irvine, CA, USA). Light intensity was measured using a radiant power meter (Ophir Photonics, North Andover, MA) and adjusted manually with a slide bar aperture.
The fish retina was stimulated with 100 ms flashes of monochromatic light at increasing irradiances until a criterion retinal response (~ 30 μV) was attained at each wavelength from 350 to 650 nm in 50 nm increments. A criterion response curve was generated by recording the irradiance (in μW s−1 cm−2) necessary to elicit the criterion response for each wavelength increment. After conversion to photon flux, the inverses of these values were normalized and plotted to generate spectral sensitivity curves. Statistical comparison of the peak wavelength sensitivity (λmax, nm) of fish from each lighting condition was performed using a 2 × 2 multifactorial ANOVA to test the effects of spectrum and time on spectral sensitivity. Assumptions (homogeneity of variances and normality of the residuals) were met for this test and all other multifactor ANOVA tests.
For fish in the intensity experiment, white-light sensitivity of the retina was tested by ERG. Following 45 min of dark adaption, fish retinas were stimulated with 100 ms flashes of white light at increasing irradiances until a criterion response (μV) was achieved. After each stimulus, the difference in voltage from the trough of the ERG a-wave to the peak of the b-wave was measured, and irradiance was increased until a criterion response 80 μV above baseline noise was attained. The irradiance (in μW s−1 cm−2) required to elicit the criterion response was converted to photons s−1 cm−2. For fish in each condition, the required irradiance was averaged and compared statistically. Following a natural log transformation of the data, an Independent Samples T-test (for which all assumptions of the data were met) was used to test the effect of light intensity on the white-light sensitivity of the retina.
The effects of light spectra on photoreceptor outer segment length and distribution were determined by immunofluorescence. Eyecups were fixed in a solution of 4% paraformaldehyde and 15% picric acid in .1 M sodium phosphate buffer. Following a minimum of 48 h of fixation, eyecups were infiltrated with 25% sucrose in .1 M Tris buffer, then embedded in Tissue-Tek. Frozen 20 μm-thick cross-sections were cut in the dorso-ventral plane on a CM1850 cryostat (Leica Biosystems, Buffalo Grove, IL, USA), thaw-mounted onto gelatin–coated glass microscope slides, and dried at room temperature overnight. Slides were then placed into fixative for 1 h, followed by four, 15 min washes in Tris-buffered saline (.5 M Trizma buffer, .9% NaCl, pH 7.4). Primary antisera were diluted in Tris-buffered saline (TBS) containing .25% λ-carrageenan, 1% bovine serum albumin, and .3% Triton X-100, and applied to the slides for overnight incubation (minimum 8 h) at room temperature. After four, 15 min rinses in TBS, slides were incubated for 1 h at room temperature in fluorophore-conjugated secondary antisera. Controls for each specimen included omission of the primary antisera, and single-labeling with each primary and secondary combination. Following four rinses in Tris-buffered saline, slides were coverslipped with Slowfade Gold mounting medium with DAPI nucleic acid label (Life Technologies, Grand Island, NY) and imaged using EZ-C1 software on a Nikon C1Si upright confocal laser-scanning microscope (Nikon Instruments, Melville, NY).
Retinas were double-labeled with well-characterized antisera against rod and cone opsins [e.g., 16, 40]. Photoreceptor subtypes were labeled using a mouse monoclonal anti-rhodopsin antibody (MAB5316, 1:500 dilution, RRID AB_2156055, EMD Millipore, Billerica, MA), and a rabbit polyclonal anti-LWS cone opsin antiserum (CERN906 1:1000 dilution, RRID inapplicable, donated by W.J. DeGrip, University of Nijmegen, Nijmegen, Netherlands). Primary antisera were labeled with secondary antisera that were conjugated to Alexa Fluor fluorescent dyes (goat anti-rabbit IgG conjugated to Alexa-488, RRID AB_143165, and goat anti-mouse IgG conjugated to Alexa-555, RRID AB_141780; Life Technologies, Grand Island, NY).
For the retina of fish from the spectral experiment, cone photoreceptor abundances (number per 50 μm linear expanse of retinal section) were counted using NIS Elements (Nikon). Cone photoreceptor abundances in the dorsal and ventral aspects of the M. atlanticus retina were compared using a Mann–Whitney U Test. Cone photoreceptor abundances and outer segment lengths were compared using a 2 × 2 multifactorial ANOVA to test the effects of spectrum and time on photoreceptor distribution. Because the M. atlanticus retina only contains ‘single’ cone photoreceptors throughout life , counting photoreceptor outer segments was an appropriate measure of photoreceptor cell abundance. For the retina of fish from the intensity experiment, photoreceptor abundances were counted considering three different metrics. In juvenile M. atlanticus, the rod photoreceptors are approximately half the length of cone photoreceptors and stacked into morphological elements known as rod bundles . Therefore, the number of cones per 50 μm linear expanse of retinal section, rod bundles per 50 μm of retinal section, and cones per of rod bundle were determined using NIS Elements (Nikon). These three measures of the M. atlanticus retina, as well as cone outer segment lengths were then compared between fish in bright and dim light conditions using three separate Independent Samples T-tests, for which all assumptions of the data were met.
Comparing cone photoreceptor abundance after the intensity experiment indicated that cone abundance per 50 μm linear expanse of retina did not significantly differ between fish in the bright and dim conditions (Fig. 4b); 9.7 cells/50 μm (s.e.m. ± .80 cells) and 9.8 cells/50 μm (s.e.m. ± .32 cells) for fish in the bright and dim conditions, respectively. Congruently, cone abundance per rod bundle and rod bundle abundance (per 50 μm linear expanse of retina) also did not differ significantly between the two conditions; 4.1 cells/50 μm (s.e.m. ± .56 cells) and 4.0 cells/50 μm (s.e.m. ± .20 cells) for fish in the bright and dim conditions, respectively. Rod bundle abundance per 50 μm linear expanse of retina did not significantly differ between fish in the bright and dim conditions: 2.9 bundles/50 μm (s.e.m. ± .33) and 3.1 bundles/50 μm (s.e.m. ± .30), respectively. Cone photoreceptor outer segment lengths did not differ between the two conditions, averaging 18.3 µm (s.e.m. ± .4) and 18.4 (s.e.m. ± .49) for fish in the bright and dim light conditions, respectively.
The goal of this study was to determine the capacity of the marine fish retina to change over short (i.e., 2–4 month) timescales in response to changes in the intensity and spectrum of environmental light. Over the full time course of fish development, retinal function is known to change between life history stages [e.g., 11–13, 15, 16, 21], the outcomes of which can be influenced by light exposure over time [23–28, 41]. Aside from studies of gene expression (e.g., ), it remained unclear if disturbances to environmental light quality could drive changes in retinal form and function between major developmental transitions (i.e., within a particular developmental stage, and particularly over very short timescales relative to the full course of development). The results of the present study indicate that photoreceptor abundance, absolute sensitivity and spectral sensitivity of the M. atlanticus retina all undergo significant change in response to light condition within a 2- to 4-month timescale during the juvenile developmental stage. These changes depend upon the intensity and spectrum of lighting conditions and length of exposure.
Retinal response to light conditions
Spectral condition was found to drive changes in the peak wavelength sensitivity (λmax) of the M. atlanticus retina. Over time, fish in the ‘red’ condition became more sensitive to long-wavelength light than fish in the ‘blue’ condition. This sensitivity difference between the fish in the two color conditions was likely driven by cone photoreceptor class redistribution in the retina, as fish from the red condition were found to have a significantly greater abundance of LWS cones relative to fish held in the blue condition. Spectral conditions also may have altered SWS cone photoreceptor abundances over time, but none of the SWS cone opsin antisera tested labeled the M. atlanticus retina.
It remains unknown whether the observed changes in LWS cone photoreceptor abundance were due to expression of new opsins within existing photoreceptor cells or neurogenesis of new cells altogether. The retinas of teleost fish grow continuously through persistant neurogenesis throughout life . During this growth, cones form at the retinal boundary, the circumferential germinal zone, while rods can form there, as well as from precursor cells throughout the retina [7, 43]. Whether the retinal changes seen in this and in other studies of retinal plasticity are due to cone cell neurogenesis in the central retina remains to be elucidated.
Exposure of M. atlanticus to different irradiance levels caused absolute (white-light) sensitivity of the retina to change substantially. Fish held in the bright light condition required twice the irradiance to produce the same retinal response as fish held in the dim light condition. Yet rod and cone photoreceptor abundance, measured per unit retinal expanse and relative to each other, did not change in response to lighting condition. The observed sensitivity difference may have been a product of a variety of cellular and biochemical mechanisms including modulation of the regeneration rate of light-sensitive visual pigment molecules in photoreceptors [e.g., 44, 45], repositioning of rod and cone outer segments, movement of melanin pigment granules in the retinal pigmented epithelium (in many non-mammalian vertebrates; [e.g., 46]), chemical (de)sensitization of the retina [e.g., 47, 48], or rewiring of the inner retina.
Plasticity of the marine fish retina
Multiple previous studies of fish retinal phenotypic plasticity demonstrate retinal change in response to altered light spectra that span the entirety of development or key developmental transitions. These studies reported structural and functional changes including the relative proportions of photoreceptor sensitivities determined by microspectrophotometry (MSP; ), relative expression of opsin genes [22, 26], behavioral measures of color sensitivity , photoreceptor morphology, and even synaptic architecture of the inner retina . More recently, studies of retinal plasticity have demonstrated changes in retinal gene expression in response to short-term changes in environmental light [31–33]. The results presented here expand upon those studies, showing that in vivo retinal sensitivity and photoreceptor distribution can change in response to acute changes in environmental light that occur within a given developmental stage, between major developmental transitions. Significant retinal change occurred in only 2–4 months within the full developmental regime of M. atlanticus that encompasses 7–10 years . These results suggest that retinal plasticity may support rapid retinal change and perhaps improved vision for survival in the face of natural and anthropogenic aquatic habitat disturbances that alter intensity and spectrum of underwater light.
Elucidating the capacity of the fish retina to change in response to altered lighting conditions is important for our understanding of fish resilience to disturbances in the marine environment. Natural and anthropogenic disturbances to marine habitats (e.g., algal blooms caused by eutrophication and storm-induced turbidity changes) can lead to significant and rapid changes in the intensity and spectrum of underwater light [29, 30]. The attenuation of light and chromatic changes associated with marine disturbances may place significant pressure on the visual systems of fish, and thus survival may depend at least in part upon the ability of fish visual systems to change rapidly . The results presented here indicate plasticity of the fish retina in response to acute changes in environmental light over a few months, only ~ 2% of the time it takes M. atlanticus to fully develop. Through a combination of changes in photoreceptor distribution and modification of retinal sensitivity, the M. atlanticus retina may be able to compensate for new lighting conditions on a timescale relevant to the ecological impact of habitat disturbance. The relatively short-term changes in sensitivity described here may allow M. atlanticus to remain efficient predators, avoid potential predators, and interact productively with conspecifics even in the face of significant, rapid environmental change.
LES and MSG conceived of the study, LES carried out data collection and analysis, and LES and MSG drafted the manuscript. Both authors read and approved the final manuscript.
We thank Mark Schweikert, James King, Emily Dawson, Dr. Kristin Kopperud, Dr. Adeljean Ho, Dr. Eric Guisbert and Dr. David Carroll for logistical support. We would like to acknowledge Gayle Duncombe, Florida Institute of Technology (FIT), for assistance with confocal microscopy, and Dr. Jon Shenker and Dr. Ralph Turingan for helpful discussion and assistance in tarpon husbandry. Publication of this article was funded in part by the Open Access Subvention Fund and the Florida Tech Libraries.
The authors declare that they have no competing interests.
Availability of data and materials
The datasets used during the present study are available in the additional material, as well as from the corresponding author on request.
Consent for publication
Ethics approval and consent to participate
All experimental protocols were approved by the Florida Institute of Technology’s animal care and use committee (Animal Welfare Assurance #141016).
Funding for this work was provided by an NSF Graduate Research Fellowship (GRFP) and by a P.E.O. International Scholar Award (both to LES). Salary support was provided to LES by the GRFP through the entirety of the study, and the P.E.O Scholar award funded equipment and supplies required by the experiments. These funding organizations had no role in the design of the study, the collection, analysis and interpretation of the data, or the writing of the manuscript.
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