Backgrounds and the evolution of visual signals.

Color signals which mediate behavioral interactions across taxa and contexts are often thought of as color 'patches' - parts of an animal that appear colorful compared to other parts of that animal. Color patches, however, cannot be considered in isolation because how a color is perceived depends on its visual background. This is of special relevance to the function and evolution of signals because backgrounds give rise to a fundamental tradeoff between color signal detectability and discriminability: as its contrast with the background increases, a color patch becomes more detectable, but discriminating variation in that color becomes more difficult. Thus, the signal function of color patches can only be fully understood by considering patch and background together as an integrated whole.

Cephalopod versus vertebrate eyes.

Vertebrates and cephalopods are the two major animal groups that view the world through sophisticated camera-type eyes. There are of course exceptions: nautiloid cephalopods have more simply built pinhole eyes. Excellent camera type eyes are also found in other animals, such as some spider groups, a few snails, and certain marine worms, but the vast majority of large camera-type eyes belong to cephalopods and vertebrates. Vertebrates and cephalopods also devote major parts of their brains to the processing of visual information. Obviously, there are differences in eye performance among cephalopods and vertebrates, but there are no major subgroups where vision seems to have low priority. The similarity in eye geometry is striking, especially between fish and coleoid cephalopods, with a hemispherical retina centred around a spherical lens. Do these similarities mean that vertebrate and cephalopod eyes are equally good? Comparing the eyes of vertebrates and cephalopods reveals many fundamental differences with surprisingly small consequences for vision, but also one difference that means that cephalopods and vertebrates do not share the same visual world.

The carotenoid redshift: Physical basis and implications for visual signaling.

Carotenoid pigments are the basis for much red, orange, and yellow coloration in nature and central to visual signaling. However, as pigment concentration increases, carotenoid signals not only darken and become more saturated but they also redshift; for example, orange pigments can look red at higher concentration. This occurs because light experiences exponential attenuation, and carotenoid-based signals have spectrally asymmetric reflectance in the visible range. Adding pigment disproportionately affects the high-absorbance regions of the reflectance spectra, which redshifts the perceived hue. This carotenoid redshift is substantial and perceivable by animal observers. In addition, beyond pigment concentration, anything that increases the path length of light through pigment causes this redshift (including optical nano- and microstructures). For example, male Ramphocelus tanagers appear redder than females, despite the same population and concentration of carotenoids, due to microstructures that enhance light-pigment interaction. This mechanism of carotenoid redshift has sensory and evolutionary consequences for honest signaling in that structures that redshift carotenoid ornaments may decrease signal honesty. More generally, nearly all colorful signals vary in hue, saturation, and brightness as light-pigment interactions change, due to spectrally asymmetrical reflectance within the visible range of the relevant species. Therefore, the three attributes of color need to be considered together in studies of honest visual signaling.

Measures and models of visual acuity in epipelagic and mesopelagic teleosts and elasmobranchs.

Eyes in low-light environments typically must balance sensitivity and spatial resolution. Vertebrate eyes with large "pixels" (e.g., retinal ganglion cells with inputs from many photoreceptors) will be sensitive but provide coarse vision. Small pixels can render finer detail, but each pixel will gather less light, and thus have poor signal relative-to-noise, leading to lower contrast sensitivity. This balance is particularly critical in oceanic species at mesopelagic depths (200-1000 m) because they experience low light and live in a medium that significantly attenuates contrast. Depending on the spatial frequency and inherent contrast of a pattern being viewed, the viewer's pupil size and temporal resolution, and the ambient light level and water clarity, a visual acuity exists that maximizes the distance at which the pattern can be discerned. We develop a model that predicts this acuity for common conditions in the open ocean, and compare it to visual acuity in marine teleost fishes and elasmobranchs found at various depths in productive and oligotrophic waters. Visual acuity in epipelagic and upper mesopelagic species aligned well with model predictions, but species at lower mesopelagic depths (> 600 m) had far higher measured acuities than predicted. This is consistent with the prediction that animals found at lower mesopelagic depths operate in a visual world consisting primarily of bioluminescent point sources, where high visual acuity helps localize targets of this kind. Overall, the results suggest that visual acuity in oceanic fish and elasmobranchs is under depth-dependent selection for detecting either extended patterns or point sources.

Dynamic light filtering over dermal opsin as a sensory feedback system in fish color change.

Dynamic color change has evolved multiple times, with a physiological basis that has been repeatedly linked to dermal photoreception via the study of excised skin preparations. Despite the widespread prevalence of dermal photoreception, both its physiology and its function in regulating color change remain poorly understood. By examining the morphology, physiology, and optics of dermal photoreception in hogfish (Lachnolaimus maximus), we describe a cellular mechanism in which chromatophore pigment activity (i.e., dispersion and aggregation) alters the transmitted light striking SWS1 receptors in the skin. When dispersed, chromatophore pigment selectively absorbs the short-wavelength light required to activate the skin's SWS1 opsin, which we localized to a morphologically specialized population of putative dermal photoreceptors. As SWS1 is nested beneath chromatophores and thus subject to light changes from pigment activity, one possible function of dermal photoreception in hogfish is to monitor chromatophores to detect information about color change performance. This framework of sensory feedback provides insight into the significance of dermal photoreception among color-changing animals.

An Investigation into the Mechanism Mediating Counterillumination in Myctophid Fishes (Myctophidae).

AbstractCounterillumination is a camouflage strategy employed primarily by mesopelagic fishes, sharks, crustaceans, and squid, which use ventral bioluminescence to obscure their silhouettes when viewed from below. Although certain counterilluminating species have been shown to control the intensity of their ventral emissions to match the background downwelling light, the feedback mechanism mediating this ability is poorly understood. One proposed mechanism involves the presence and use of eye-facing photophores that would allow simultaneous detection and comparison of photophore emissions and downwelling solar light. Eye-facing photophores have been found in at least 34 species of counterilluminating stomiiform fishes and the myctophid Tarletonbeania crenularis. Here, we examined nine phylogenetically spaced myctophid species for eye-facing photophores to assess whether this mechanism is as prevalent in this group as it is in the Stomiiformes. First, microcomputed tomography imaging data were collected for each species, and three-dimensional reconstructions of the fishes were developed to identify potential eye-facing photophores. The fishes were then dissected under a stereomicroscope to confirm the presence of all identified photophores, probe for any photophores missed in the reconstruction analysis, and determine the orientation of the photophores' emissions. Although photophores were identified near the orbits of all species examined, none of the fishes' photophores directed light into their orbits, suggesting that myctophids may regulate bioluminescence through an alternative mechanism.

Glassfrogs conceal blood in their liver to maintain transparency.

Transparency in animals is a complex form of camouflage involving mechanisms that reduce light scattering and absorption throughout the organism. In vertebrates, attaining transparency is difficult because their circulatory system is full of red blood cells (RBCs) that strongly attenuate light. Here, we document how glassfrogs overcome this challenge by concealing these cells from view. Using photoacoustic imaging to track RBCs in vivo, we show that resting glassfrogs increase transparency two- to threefold by removing ~89% of their RBCs from circulation and packing them within their liver. Vertebrate transparency thus requires both see-through tissues and active mechanisms that "clear" respiratory pigments from these tissues. Furthermore, glassfrogs' ability to regulate the location, density, and packing of RBCs without clotting offers insight in metabolic, hemodynamic, and blood-clot research.

Collective movement as a solution to noisy navigation and its vulnerability to population loss.

Many animals use the geomagnetic field to migrate long distances with high accuracy; however, research has shown that individual responses to magnetic cues can be highly variable. Thus, it has been hypothesized that magnetoreception alone is insufficient for accurate migrations and animals must either switch to a more accurate sensory cue or integrate their magnetic sense over time. Here we suggest that magnetoreceptive migrators could also use collective navigation strategies. Using agent-based models, we compare agents utilizing collective navigation to both the use of a secondary sensory system and time-integration. Our models demonstrate that collective navigation allows for 70% success rates for noisy navigators. To reach the same success rates, a secondary sensory system must provide perfect navigation for over 73% of the migratory route, and time integration must integrate over 50 time-steps, indicating that magnetoreceptive animals could benefit from using collective navigation. Finally, we explore the impact of population loss on animals relying on collective navigation. We show that as population density decreases, a greater proportion of individuals fail to reach their destination and that a 50% population reduction can result in up to a 37% decrease in the proportion of individuals completing their migration.

The movement ecology of fishes.

Movement of fishes in the aquatic realm is fundamental to their ecology and survival. Movement can be driven by a variety of biological, physiological and environmental factors occurring across all spatial and temporal scales. The intrinsic capacity of movement to impact fish individually (e.g., foraging) with potential knock-on effects throughout the ecosystem (e.g., food web dynamics) has garnered considerable interest in the field of movement ecology. The advancement of technology in recent decades, in combination with ever-growing threats to freshwater and marine systems, has further spurred empirical research and theoretical considerations. Given the rapid expansion within the field of movement ecology and its significant role in informing management and conservation efforts, a contemporary and multidisciplinary review about the various components influencing movement is outstanding. Using an established conceptual framework for movement ecology as a guide (i.e., Nathan et al., 2008: 19052), we synthesized the environmental and individual factors that affect the movement of fishes. Specifically, internal (e.g., energy acquisition, endocrinology, and homeostasis) and external (biotic and abiotic) environmental elements are discussed, as well as the different processes that influence individual-level (or population) decisions, such as navigation cues, motion capacity, propagation characteristics and group behaviours. In addition to environmental drivers and individual movement factors, we also explored how associated strategies help survival by optimizing physiological and other biological states. Next, we identified how movement ecology is increasingly being incorporated into management and conservation by highlighting the inherent benefits that spatio-temporal fish behaviour imbues into policy, regulatory, and remediation planning. Finally, we considered the future of movement ecology by evaluating ongoing technological innovations and both the challenges and opportunities that these advancements create for scientists and managers. As aquatic ecosystems continue to face alarming climate (and other human-driven) issues that impact animal movements, the comprehensive and multidisciplinary assessment of movement ecology will be instrumental in developing plans to guide research and promote sustainability measures for aquatic resources.

Testing Mechanisms of Vision: Sea Urchin Spine Density Does Not Correlate With Vision-Related Environmental Characteristics.

Sea urchins do not have eyes, yet they are capable of resolving simple images. One suggestion as to the mechanism of this capability is that the spines shade off-axis light from reaching the photosensitive test (skeleton). Following this hypothesis, the density of spines across the body determines the resolution (or sharpness) of vision by restricting the incidence of light on the photosensitive skin of the animal, creating receptive areas of different minimum resolvable angles. Previous studies have shown that predicted resolutions in several species closely match behaviorally-determined resolutions, ranging from 10º to 33º. Here we present a comparative morphological survey of spine density with species representatives from 22 of the 24 families of regular sea urchins (Class Echinoidea) in order to better understand the relative influences of phylogenetic history and three visually-relevant environmental variables on this trait. We estimated predicted resolutions by calculating spine densities from photographs of spineless sea urchin tests (skeletons). Analyses showed a strong phylogenetic signal in spine density differences between species. Phylogenetically-corrected Generalized Least Squares (PGLS) models incorporating all habitat parameters were the most supported, and no particular parameter was significantly correlated with spine density. Spine density is subject to multiple, overlapping selective pressures and therefore it is possible that either: 1) spine density does not mediate spatial vision in echinoids, or 2) visual resolution via spine density is a downstream consequence of sea urchin morphology rather than a driving force of adaptation in these animals.

Influence of visual background on discrimination of signal-relevant colours in zebra finches (Taeniopygia guttata).

Colour signals of many animals are surrounded by a high-contrast achromatic background, but little is known about the possible function of this arrangement. For both humans and non-human animals, the background colour surrounding a colour stimulus affects the perception of that stimulus, an effect that can influence detection and discrimination of colour signals. Specifically, high colour contrast between the background and two given colour stimuli makes discrimination more difficult. However, it remains unclear how achromatic background contrast affects signal discrimination in non-human animals. Here, we test whether achromatic contrast between signal-relevant colours and an achromatic background affects the ability of zebra finches to discriminate between those colours. Using an odd-one-out paradigm and generalized linear mixed models, we found that higher achromatic contrast with the background, whether positive or negative, decreases the ability of zebra finches to discriminate between target and non-target stimuli. This effect is particularly strong when colour distances are small (less than 4 ΔS) and Michelson achromatic contrast with the background is high (greater than 0.5). We suggest that researchers should consider focal colour patches and their backgrounds as collectively comprising a signal, rather than focusing on solely the focal colour patch itself.

Macropinna.

Sönke Johnsen and Steve Haddock introduce the remarkable deep-sea fish Macropinna microstoma whose transparent head and rotating tubular eyes are two novel adaptations that allow it to see and hunt at depth.

Environmental sources of radio frequency noise: potential impacts on magnetoreception.

Radio frequency electromagnetic noise (RF) of anthropogenic origin has been shown to disrupt magnetic orientation behavior in some animals. Two sources of natural RF might also have the potential to disturb magnetic orientation behavior under some conditions: solar RF and atmospheric RF. In this review, we outline the frequency ranges and electric/magnetic field magnitudes of RF that have been shown to disturb magnetoreceptive behavior in laboratory studies and compare these to the ranges of solar and atmospheric RF. Frequencies shown to be disruptive in laboratory studies range from 0.1 to 10 MHz, with magnetic magnitudes as low as 1 nT reported to have effects. Based on these values, it appears unlikely that solar RF alone routinely disrupts magnetic orientation. In contrast, atmospheric RF does sometimes exceed the levels known to disrupt magnetic orientation in laboratory studies. We provide a reference for when and where atmospheric RF can be expected to reach these levels, as well as a guide for quantifying RF measurements.

The sensory impacts of climate change: bathymetric shifts and visually mediated interactions in aquatic species.

Visual perception is, in part, a function of the ambient illumination spectrum. In aquatic environments, illumination depends upon the water's optical properties and depth, both of which can change due to anthropogenic impacts: turbidity is increasing in many aquatic habitats, and many species have shifted deeper in response to warming surface waters (known as bathymetric shifts). Although increasing turbidity and bathymetric shifts can result in similarly large changes to a species' optical environment, no studies have yet examined the impact of the latter on visually mediated interactions. Here, we examine a potential link between climate change and visual perception, with a focus on colour. We discuss (i) what is known about bathymetric shifts; (ii) how the impacts of bathymetric shifts on visual interactions may be distributed across species; (iii) which interactions might be affected; and (iv) the ways that animals have to respond to these changes. As warming continues and temperature fluctuations grow more extreme, many species may move into even deeper waters. There is thus a need for studies that examine how such shifts can affect an organism's visual world, interfere with behaviour, and impact fitness, population dynamics, and community structure.

Comparison of Categorical Color Perception in Two Estrildid Finches.

AbstractSensory systems are predicted to be adapted to the perception of important stimuli, such as signals used in communication. Prior work has shown that female zebra finches perceive the carotenoid-based orange-red coloration of male beaks-a mate choice signal-categorically. Specifically, females exhibited an increased ability to discriminate between colors from opposite sides of a perceptual category boundary than equally different colors from the same side of the boundary. The Bengalese finch, an estrildid finch related to the zebra finch, is black, brown, and white, lacking carotenoid coloration. To explore the relationship between categorical color perception and signal use, we tested Bengalese finches using the same orange-red continuum as in zebra finches, and we also tested how both species discriminated among colors differing systematically in hue and brightness. Unlike in zebra finches, we found no evidence of categorical perception of an orange-red continuum in Bengalese finches. Instead, we found that the combination of chromatic distance (hue difference) and Michelson contrast (difference in brightness) strongly correlated with color discrimination ability on all tested color pairs in Bengalese finches. The pattern was different in zebra finches: this strong correlation held when discriminating between colors from different categories but not when discriminating between colors from within the same category. These experiments suggest that categorical perception is not a universal feature of avian-or even estrildid finch-vision. Our findings also provide further insights into the mechanism underlying categorical perception and are consistent with the hypothesis that categorical perception is adapted for signal perception.

The orbital hoods of snapping shrimp have surface features that may represent tradeoffs between vision and protection.

Snapping shrimp (Alpheidae) are decapod crustaceans named for the snapping claws with which they produce cavitation bubbles. Snapping shrimp use the shock waves released by collapsing cavitation bubbles as weapons. Along with their distinctive claws, snapping shrimp have orbital hoods, extensions of their carapace that cover their heads and eyes. Snapping shrimp view the world through their orbital hoods, so we asked if the surfaces of the orbital hoods of the snapping shrimp Alpheus heterochaelis have features that minimize the scattering of light. Using SEM, we found that surface features, primarily microbial epibionts, covered less space on the surfaces of the orbital hoods of A. heterochaelis (∼18%) than they do elsewhere on the carapace (∼50%). Next, we asked if these surface features influence aerophobicity. By measuring the contact angles of air bubbles, we found the orbital hoods of A. heterochaelis are less aerophobic than other regions of the carapace. Surfaces that are less aerophobic are more likely to have cavitation bubbles adhere to them and are more likely to have shock waves cause new cavitation bubbles to nucleate upon them. Computational modeling indicates the orbital hoods of A. heterochaelis face a functional trade-off: fewer surface features, such as less extensive communities of microbial epibionts, may minimize the scattering of light at the cost of making the adhesion and nucleation of cavitation bubbles more likely.

The visual ecology of selective predation: Are unhealthy hosts less stealthy hosts?

Predators can strongly influence disease transmission and evolution, particularly when they prey selectively on infected hosts. Although selective predation has been observed in numerous systems, why predators select infected prey remains poorly understood. Here, we use a mathematical model of predator vision to test a long-standing hypothesis about the mechanistic basis of selective predation in a Daphnia-microparasite system, which serves as a model for the ecology and evolution of infectious diseases. Bluegill sunfish feed selectively on Daphnia infected by a variety of parasites, particularly in water uncolored by dissolved organic carbon. The leading hypothesis for selective predation in this system is that infection-induced changes in the transparency of Daphnia render them more visible to bluegill. Rigorously evaluating this hypothesis requires that we quantify the effect of infection on the visibility of prey from the predator's perspective, rather than our own. Using a model of the bluegill visual system, we show that three common parasites, Metschnikowia bicuspidata, Pasteuria ramosa, and Spirobacillus cienkowskii, decrease the transparency of Daphnia, rendering infected Daphnia darker against a background of bright downwelling light. As a result of this increased brightness contrast, bluegill can see infected Daphnia at greater distances than uninfected Daphnia-between 19% and 33% further, depending on the parasite. Pasteuria and Spirobacillus also increase the chromatic contrast of Daphnia. These findings lend support to the hypothesis that selective predation by fish on infected Daphnia could result from the effects of infection on Daphnia's visibility. However, contrary to expectations, the visibility of Daphnia was not strongly impacted by water color in our model. Our work demonstrates that models of animal visual systems can be useful in understanding ecological interactions that impact disease transmission.

Novel mitochondrial derived Nuclear Excisosome degrades nuclei during differentiation of prosimian Galago (bush baby) monkey lenses.

The unique cellular organization and transparent function of the ocular lens depend on the continuous differentiation of immature epithelial cells on the lens anterior surface into mature elongated fiber cells within the lens core. A ubiquitous event during lens differentiation is the complete elimination of organelles required for mature lens fiber cell structure and transparency. Distinct pathways have been identified to mediate the elimination of non-nuclear organelles and nuclei. Recently, we reported the discovery of a unique structure in developing fiber cells of the chick embryo lens, called the Nuclear Excisosome, that is intractably associated with degrading nuclei during lens fiber cell differentiation. In the chick lens, the Nuclear Excisosome is derived from projections of adjacent cells contacting the nuclear envelope during nuclear elimination. Here, we demonstrate that, in contrast to the avian model, Nuclear Excisosomes in a primate model, Galago (bush baby) monkeys, are derived through the recruitment of mitochondria to form unique linear assemblies that define a novel primate Nuclear Excisosome. Four lenses from three monkeys aged 2-5 years were fixed in formalin, followed by paraformaldehyde, then processed for Airyscan confocal microscopy or transmission electron microscopy. For confocal imaging, fluorescent dyes labelled membranes, carbohydrate in the extracellular space, filamentous actin and nuclei. Fiber cells from Galago lenses typically displayed prominent linear structures within the cytoplasm with a distinctive cross-section of four membranes and lengths up to 30 µm. The outer membranes of these linear structures were observed to attach to the outer nuclear envelope membrane to initiate degradation near the organelle-free zone. The origin of these unique structures was mitochondria in the equatorial epithelium (not from plasma membranes of adjacent cells as in the chick embryo model). Early changes in mitochondria appeared to be the collapse of the cristae and modification of one side of the mitochondrial outer membrane to promote accumulation of protein in a dense cluster. As a mitochondrion surrounded the dense protein cluster, an outer mitochondrial membrane enclosed the protein to form a core and another outer mitochondrial membrane formed the outermost layer. The paired membranes of irregular texture between the inner core membrane and the outer limiting membrane appeared to be derived from modified mitochondrial cristae. Several mitochondria were involved in the formation and maturation of these unique complexes that apparently migrated around the fulcrum into the cytoplasm of nascent fiber cells where they were stabilized until the nuclear degradation was initiated. Thus, unlike in the chick embryo, the Galago lenses degraded nuclear envelopes with a Nuclear Excisosome derived from multiple mitochondria in the epithelium that formed novel linear assemblies in developing fiber cells. These findings suggest that recruitment of distinct structures is required for Nuclear Excisosome formation in different species.

Visual perception of light organ patterns in deep-sea shrimps and implications for conspecific recognition.

Darkness and low biomass make it challenging for animals to find and identify one another in the deep sea. While spatiotemporal variation in bioluminescence is thought to underlie mate recognition for some species, its role in conspecific recognition remains unclear. The deep-sea shrimp genus, Sergestes sensu lato (s.l.), is one group that is characterized by species-specific variation in light organ arrangement, providing us the opportunity to test whether organ variation permits recognition to the species level. To test this, we analyzed the visual capabilities of three species of Sergestes s.l. in order to (a) test for sexual dimorphism in eye-to-body size scaling relationships, (b) model the visual ranges (i.e., sighting distances) over which these shrimps can detect intraspecific bioluminescence, and (c) assess the maximum possible spatial resolution of the eyes of these shrimps to estimate their capacity to distinguish the light organs of each species. Our results showed that relative eye size scaled negatively with body length across species and without sexual dimorphism. Though the three species appear capable of detecting one another's bioluminescence over distances ranging from < 1 to ~6 m, their limited spatial resolution suggests they cannot resolve light organ variation for the purpose of conspecific recognition. Our findings point to factors other than conspecific recognition (e.g., neutral drift, phenotypic constraint) that have led to the extensive diversification of light organs in Sergestes s.l and impart caution about interpreting ecological significance of visual characters based on the resolution of human vision. This work provides new insight into deep-sea animal interaction, supporting the idea that-at least for these mesopelagic shrimps-nonvisual signals may be required for conspecific recognition.