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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.

Synopsis 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 10° to 33°. 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 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.

Many animals use assessment signals to resolve contests over limited resources while minimizing the costs of those contests. The carotenoid-based orange to red bills of male zebra finches (Taeniopygia guttata) are thought to function as assessment signals in male-male contests, but behavioral analyses relating contest behaviors and outcomes to bill coloration have yielded mixed results. We examined the relationship between bill color and contests while incorporating measurements of color perception and testosterone (T) production, for an integrative view of aggressive signal behavior, production, and perception. We assayed the T production capabilities of 12 males in response to a gonadotropin-releasing hormone (GnRH) challenge. We then quantified the initiation, escalation, and outcome of over 400 contests in the group, and measured bill color using calibrated photography. Finally, because signal perception can influence signal function, we tested how males perceive variation in bill coloration, asking if males exhibit categorical perception of bill color, as has been shown recently in female zebra finches. The data suggest that males with greater T production capabilities than their rivals were more likely to initiate contests against those rivals, while males with redder bills than their rivals were more likely to win contests. Males exhibited categorical color perception, but individual variation in the effect of categorical perception on color discrimination abilities did not predict any aspects of contest behavior or outcomes. Our results are consistent with the hypotheses that T plays a role in zebra finch contests and that bill coloration functions as an aggressive signal. We suggest future approaches, based on animal contest theory, for how links among signals, perception, and assessment can be tested.

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.

Sensory 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.

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.

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, have 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 PNAS. 105:19052), we synthesize 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 explore how associated strategies help survival by optimizing physiological and other biological states. Next, we identify 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 consider 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.

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.

More than 100 years ago, the biologist Jakob von Uexküll suggested that, because sensory systems are diverse, animals likely inhabit different sensory worlds (umwelten) than we do. Since von Uexküll, work across sensory modalities has confirmed that animals sometimes perceive sensory information that humans cannot, and it is now well-established that one must account for this fact when studying an animal’s behavior. We are less adept, however, at recognizing cases in which non-human animals may not detect or perceive stimuli the same way we do, which is our focus here. In particular, we discuss three ways in which our own perception can result in misinformed hypotheses about the function of various stimuli. In particular, we may (1) make untested assumptions about how sensory information is perceived, based on how we perceive or measure it, (2) attribute undue significance to stimuli that we perceive as complex or striking, and (3) assume that animals divide the sensory world in the same way that we as scientists do. We discuss each of these biases and provide examples of cases where animals cannot perceive or are not attending to stimuli in the same way that we do, and how this may lead us to mistaken assumptions. Because what an animal perceives affects its behavior, we argue that these biases are especially important for researchers in sensory ecology, cognition, and animal behavior and communication to consider. We suggest that studying animal umwelten requires integrative approaches that combine knowledge of sensory physiology with behavioral assays.

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.

Made available in DSpace on 2021-06-25T12:20:40Z (GMT). No. of bitstreams: 0 Previous issue date: 2020-08-04 Human Frontier Science Program Consejo Nacional de Investigaciones Cientificas y Tecnicas (CONICET) Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) Agencia Nacional de Promocion Cientifica y Tecnologica, Proyecto de Investigacion Cientifica y Tecnologica CONICET Universidad de Buenos Aires Universidad de Buenos Aires Ciencia y Tecnica Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) Secretaria Nacional de Educacion Superior, Ciencia, Tecnologia e Innovacion del Ecuador (SENESCYT) (Arca de Noe initiative) Direccion General Academica Pontificia Universidad Catolica del Ecuador Many vertebrates have distinctive blue-green bones and other tissues due to unusually high biliverdin concentrations-a phenomenon called chlorosis. Despite its prevalence, the biochemical basis, biology, and evolution of chlorosis are poorly understood. In this study, we show that the occurrence of high biliverdin in anurans (frogs and toads) has evolved multiple times during their evolutionary history, and relies on the same mechanism-the presence of a class of serpin family proteins that bind biliverdin. Using a diverse combination of techniques, we purified these serpins from several species of nonmodel treefrogs and developed a pipeline that allowed us to assemble their complete amino acid and nucleotide sequences. The described proteins, hereafter named biliverdin-binding serpins (BBS), have absorption spectra that mimic those of phytochromes and bacteriophytochromes. Our models showed that physiological concentration of BBS5 fine-tune the color of the animals, providing the physiological basis for crypsis in green foliage even under near-infrared light. Additionally, we found that these BBS5 are most similar to human glycoprotein alpha-1-antitrypsin, but with a remarkable functional diversification. Our results present molecular and functional evidence of recurrent evolution of chlorosis, describe a biliverdin-binding protein in vertebrates, and introduce a function for a member of the serpin superfamily, the largest and most ubiquitous group of protease inhibitors. Duke Univ, Dept Biol, Durham, NC 27708 USA Consejo Nacl Invest Cient & Tecn CONICET, Museo Argentino Ciencias Nat Bernardino Rivadavia, Div Herpetol, C1405DJR, Buenos Aires, DF, Argentina Univ Buenos Aires, Fac Ciencias Exactas & Nat, Inst Quim Fis Mat Medio Ambiente & Energia, Consejo Nacl Invest Cient & Tecn CONICET, C1428EHA, Buenos Aires, DF, Argentina Univ Sao Paulo, Fac Ciencias Farmaceut Ribeirao Preto, Dept Ciencias BioMol, Nucleo Pesquisa Prod Nat & Sintet NPPNS, BR-14040903 Ribeirao Preto, SP, Brazil Univ Nacl Misiones, Fac Ciencias Exactas, Inst Biol Subtrop CONICET UNaM, Lab Genet Evolut Claudio Juan Bidau, RA-3300 Posadas, Misiones, Argentina Univ Estadual Paulista, Dept Biodiversidade, BR-13506900 Rio Claro, SP, Brazil Univ Estadual Paulista, Ctr Aquicultura, Inst Biociencias, BR-13506900 Rio Claro, SP, Brazil Univ Cent Florida, Dept Biol Genom & Bioinformat Cluster, Orlando, FL 32816 USA Pontificia Univ CatOlica Ecuador, Escuela Biol, Museo Zool, Aptdo 17-01-2184, Quito, Ecuador Univ Buenos Aires, Fac Ciencias Exactas & Nat, Dept Quim Inorgan Analit & Quim Fis, C1428EHA, Buenos Aires, DF, Argentina Univ Buenos Aires, Fac Ciencias Exactas & Nat, Dept Biodiversidad & Biol Expt, C1428EHA, Buenos Aires, DF, Argentina Consejo Nacl Invest Cient & Tecn, Fdn Inst Leloir, C1405BWE, Buenos Aires, DF, Argentina Consejo Nacl Invest Cient & Tecn, Inst Invest Bioquim Buenos Aires, C1405BWE, Buenos Aires, DF, Argentina Univ Nacl San Martin, Inst Invest Biotecnol, RA-1650 San Martin, Buenos Aires, Argentina Univ Estadual Paulista, Dept Biodiversidade, BR-13506900 Rio Claro, SP, Brazil Univ Estadual Paulista, Ctr Aquicultura, Inst Biociencias, BR-13506900 Rio Claro, SP, Brazil Human Frontier Science Program: LT 000660/2018-L FAPESP: 2014/20915-6 FAPESP: 2017/23725-1 FAPESP: 2017/26162-8 Agencia Nacional de Promocion Cientifica y Tecnologica, Proyecto de Investigacion Cientifica y Tecnologica: 2011-1895 Agencia Nacional de Promocion Cientifica y Tecnologica, Proyecto de Investigacion Cientifica y Tecnologica: 2013-404 Agencia Nacional de Promocion Cientifica y Tecnologica, Proyecto de Investigacion Cientifica y Tecnologica: 2013-1895 Agencia Nacional de Promocion Cientifica y Tecnologica, Proyecto de Investigacion Cientifica y Tecnologica: 2014-1022 Agencia Nacional de Promocion Cientifica y Tecnologica, Proyecto de Investigacion Cientifica y Tecnologica: 2015-820 CONICET: 11220150100394CO Universidad de Buenos Aires Ciencia y Tecnica: 20020170100037BA FAPESP: 2013/50741-7 FAPESP: 2012/10000-5 FAPESP: 2014/50342-8 FAPESP: 2018/15425-0 CNPq: 306623/2018-8

Abstract In the context of mate choice, males may vary continuously in their expression of assessment signals, typically reflecting information about variation in mate quality. Similarly, females may exhibit variation in mate preference, which could be due to differences in how individual females perceive signals. The extent to which perception varies across individuals, however, and whether differences in sensory physiology underlie perceptual differences is poorly understood. Carotenoid pigments create the orange-red coloration of many assessment signals, and they also play a role in color discrimination in many vertebrates via their presence in retinal oil droplets. Here, we link variation in oil droplet carotenoid concentration with the ability of female zebra finches (Taeniopygia guttata) to discriminate an orange-red color continuum that parallels variation in male beak color, a mate assessment signal. We have shown previously that zebra finch females perceive this color range categorically, meaning they label color stimuli from this continuum as belonging to two categories and exhibit better discrimination between colors from different categories as compared with equally different colors from within a category. We quantified behavioral color discrimination and R-type (red) cone oil droplet spectral absorption, a proxy for carotenoid concentration. Oil droplet absorption was strongly predictive of variation in behavioral color discrimination ability. In particular, higher carotenoid concentration in oil droplets correlated with increased discrimination of colors from different sides of the previously identified category boundary. These data show that differences in the sensory periphery can correlate with individual variation in perception of a signal-relevant color range. Significance statement Signal receivers vary in their preferences for signaling traits, but whether this is due to variation in how different receivers perceive signals is not well-understood. We show that variation between individual zebra finch females in perception of an orange-red continuum range correlates with the carotenoid concentration of retinal oil droplets. These data provide the first direct evidence that individual variation in oil droplet carotenoid concentration can lead to variation in color discrimination ability. Linking variation in signal-relevant color discrimination ability with variation in retinal physiology suggests a potential mechanism contributing to individual variation in signal assessment.

Counterillumination, the masking of an animal's silhouette with ventral photophores, is found in a number of mesopelagic taxa but is difficult to employ because it requires that the animal match the intensity of downwelling light without seeing its own ventral photophores. It has been proposed that the myctophid,Tarletonbeania crenularis,uses a photophore directed towards the eye, termed an eye-facing photophore, as a reference standard that it adjusts to match downwelling light. The potential use of this mechanism, however, has not been evaluated in other fishes. Here, we use micro-computed tomography, photography and dissection to evaluate the presence/absence of eye-facing photophores in three families of stomiiform fishes. We found that all sampled species with ventral photophores capable of counterillumination possess an eye-facing photophore that is pigmented on the anterior and lateral sides, thus preventing its use as a laterally directed signal, lure or searchlight. The two species that are incapable of counterillumination,Cyclothone obscuraandSigmops bathyphilus, lack an eye-facing photophore. After determining the phylogenetic distribution of eye-facing photophores, we used histology to examine the morphology of the cranial tissue inArgyropelecus aculeatusand determined that light from the eye-facing photophore passes through a transparent layer of tissue, then the lens, and finally strikes the accessory retina. Additionally, eight of the 14 species for which fresh specimens were available had an aphakic gap that aligned with the path of emitted light from the eye-facing photophore, while the remaining six had no aphakic gap. These findings, combined with records of eye-facing photophores from distantly related taxa, strongly suggest that eye-facing photophores serve as a reference for counterillumination in these fishes.

At oceanic depths200 m, there is little ambient sunlight, but bioluminescent organisms provide another light source that can reveal animals to visual predators and prey [1-4]. Transparency and mirrored surfaces-common camouflage strategies under the diffuse solar illumination of shallower waters-are conspicuous when illuminated by directed bioluminescent sources due to reflection from the body surface [5, 6]. Pigmentation allows animals to absorb light from bioluminescent sources, rendering them visually undetectable against the dark background of the deep sea [5]. We present evidence suggesting pressure to reduce reflected bioluminescence led to the evolution of ultra-black skin (reflectance0.5%) in 16 species of deep-sea fishes across seven distantly related orders. Histological data suggest this low reflectance is mediated by a continuous layer of densely packed melanosomes in the exterior-most layer of the dermis [7, 8] and that this layer lacks the unpigmented gaps between pigment cells found in other darkly colored fishes [9-13]. Using finite-difference, time-domain modeling and comparisons with melanosomes found in other ectothermic vertebrates [11, 13-21], we find the melanosomes making up the layer in these ultra-black species are optimized in size and shape to minimize reflectance. Low reflectance results from melanosomes scattering light within the layer, increasing the optical path length and therefore light absorption by the melanin. By reducing reflectance, ultra-black fish can reduce the sighting distance of visual predators more than 6-fold compared to fish with 2% reflectance. This biological example of efficient light absorption via a simple architecture of strongly absorbing and highly scattering particles may inspire new ultra-black materials.

Rod spectral sensitivity data (λmax ), measured by microspectrophotometry, were compiled for 403 species of ray-finned fishes in order to examine four hypothesized predictors of rod spectral sensitivity (depth, habitat, diet and temperature). From this database, a subset of species that were known to be adults and available on a published phylogeny (n = 210) were included in analysis, indicating rod λmax values averaging 503 nm and ranging from 477 to 541 nm. Linear models that corrected for phylogenetic relatedness showed that variation in rod sensitivity was best predicted by habitat and depth, with shorter wavelength λmax values occurring in fishes found offshore or in the deep sea. Neither diet, nor the interaction of diet and habitat, had significant explanatory power. Although temperature significantly correlated with rod sensitivity, in that fishes in temperate latitudes had longer wavelength rod λmax values than those in tropical latitudes, sampling inequity and other confounds require the role of the temperature to be studied further. Together, these findings indicate that fish rod λmax is influenced by several ecological factors, suggesting that selection can act on even small differences in fish spectral sensitivity.

Whole-body transparency, an effective camouflage strategy in many aquatic species, can be disrupted by environmental and/or physiological stressors. We found that tail-flip escape responses temporarily disrupt the transparency of the anemone shrimp Ancylomenes pedersoni. After as few as three tail flips, the previously transparent abdominal muscle became cloudy. Eliciting additional tail flips to the point of exhaustion (16±1 s.e.m.; n=23) resulted in complete opacity, though the original transparency returned after 20–60 min of inactivity. We hypothesized that an exercise-induced increase in blood volume between muscle fibers creates regions of low refractive index fluid between high refractive index muscles, thereby increasing light scattering. We documented pre- and post-contraction perfusion by injecting Alexa Fluor 594 wheat germ agglutinin that labeled sarcolemmal surfaces and endothelial cells in contact with hemolymph and found more hemolymph perfused through the abdominal tissue post-exercise, presumably owing to more capillaries opening. In addition, we altered salinity (to 55‰ and 8‰), perforated the abdomen and injected a vasodilator. All three treatments increased both perfusion and opacity, lending further support to our hypothesis that increased hemolymph perfusion to the abdomen is one mechanism that can disrupt a shrimp's transparency. The fact that transparent shrimp at rest have little to no evidence of perfusion to their abdominal musculature (unlike the opaque shrimp Lysmata pederseni, which had more perfusion even at rest) indicates that they may experience significant physiological trade-offs in order to maintain their transparency; specifically, limiting blood flow and thereby reducing oxygen delivery may result in reduced performance.

1.Visual acuity is one of three basic parameters that characterize a visual system. However, few comparative studies of signals, camouflage, and ecology in general have considered visual acuity. This is unfortunate, because humans have high acuity, and thus researchers may focus on visual details of animals and habitats that are not actually visible to the relevant species. 2.Here we present AcuityView, a package for use in the software R which uses Fourier methods, measures of a viewer's acuity, viewing distance, and the size of an image to modify images. 3.AcuityView renders an image in a way that preserves only the information that an animal with a given visual acuity can detect at a certain distance, thus displaying an image that shows only the visual information available to that viewer. 4Ultimately, this will allow for a more informed analysis of what aspects of an animal's visual world may be detectable, and thus relevant to their ecology. This article is protected by copyright. All rights reserved.

Evidence from live gray whale strandings suggests that their navigation may be disrupted by increased radio frequency noise generated by solar storms, suggesting the potential for magnetoreception in this species.

In many contexts, animals assess each other using signals that vary continuously across individuals and, on average, reflect variation in the quality of the signaller1,2. It is often assumed that signal receivers perceive and respond continuously to continuous variation in the signal2. Alternatively, perception and response may be discontinuous3, owing to limitations in discrimination, categorization or both. Discrimination is the ability to tell two stimuli apart (for example, whether one can tell apart colours close to each other in hue). Categorization concerns whether stimuli are grouped based on similarities (for example, identifying colours with qualitative similarities in hue as similar even if they can be distinguished)4. Categorical perception is a mechanism by which perceptual systems categorize continuously varying stimuli, making specific predictions about discrimination relative to category boundaries. Here we show that female zebra finches (Taeniopygia guttata) categorically perceive a continuously variable assessment signal: the orange to red spectrum of male beak colour. Both predictions of categorical perception5 were supported: females (1) categorized colour stimuli that varied along a continuum and (2) showed increased discrimination between colours from opposite sides of a category boundary compared to equally different colours from within a category. To our knowledge, this is the first demonstration of categorical perception of signal-based colouration in a bird, with implications for understanding avian colour perception and signal evolution in general.

The bay scallop Argopecten irradians (Mollusca: Bivalvia) has dozens of iridescent blue eyes that focus light using mirror-based optics. Here, we test the hypothesis that these eyes appear blue because of photonic nanostructures that preferentially scatter short-wavelength light. Using transmission electron microscopy, we found that the epithelial cells covering the eyes of A. irradians have three distinct layers: an outer layer of microvilli, a middle layer of random close-packed nanospheres and an inner layer of pigment granules. The nanospheres are approximately 180 nm in diameter and consist of electron-dense cores approximately 140 nm in diameter surrounded by less electron-dense shells 20 nm thick. They are packed at a volume density of approximately 60% and energy-dispersive X-ray spectroscopy indicates that they are not mineralized. Optical modelling revealed that the nanospheres are an ideal size for producing angle-weighted scattering that is bright and blue. A comparative perspective supports our hypothesis: epithelial cells from the black eyes of the sea scallop Placopecten magellanicus have an outer layer of microvilli and an inner layer of pigment granules but lack a layer of nanospheres between them. We speculate that light-scattering nanospheres help to prevent UV wavelengths from damaging the internal structures of the eyes of A. irradians and other blue-eyed scallops.

In cleaning mutualisms, small cleaner organisms remove ectoparasites and dead skin from larger clients. Because cheating by predatory clients can result in cleaner death, cleaners should assess the potential risk of interacting with a given client and adjust their behaviour accordingly. Cleaner shrimp are small marine crustaceans that interact with numerous client fish species, many of which are potential predators. We use in situ observations of cleaner–client interactions to show that the cleaner shrimp Lysmata amboinensis adjusts several behaviours when interacting with predatory versus non-predatory clients. Predatory clients were cleaned in a significantly lower proportion of interactions than non-predatory clients, and cleaners also exhibited a leg rocking behaviour—potentially signalling their identity or intent to clean—almost exclusively toward predatory clients. Incidence of leg rocking was positively correlated with client size, and laboratory experiments showed that it can be elicited by dark visual stimuli and decreases in illumination level. Thus, cleaners clean less frequently when predation risk is higher, and may use leg rocking as a signal advertising cleaning services and directed specifically at predators.

The legend of the “kraken” has captivated humans for millennia, yet our knowledge of the large deep-sea cephalopods that inspired this myth remains limited. Conventional methods for exploring the deep sea, including the use of nets, manned submersibles, and remotely operated vehicles (ROVs), are primarily suited for studying slow-moving or sessile organisms, and baited camera-traps tend to attract scavengers rather than predators. To address these issues, unobtrusive deep-sea camera platforms were developed that used low-light cameras, red illuminators, and bioluminescence-mimicking lures. Here, we report on several opportunistic deployments of these devices in the Wider Caribbean Region where we recorded several encounters with large deep-sea squids, including the giant squid Architeuthis dux Steenstrup 1857, Pholidoteuthis adami Voss 1956, and two large squid that may be Promachoteuthis sp. (possibly P. sloani Young et al. 2006). These species were recorded between depths of 557 and 950 m. We estimate the Mantle Lengths (ML) of Promachoteuthis were ~1.0 m, the ML of the Pholidoteuthis was ~0.5 m, and the ML of the Archtiteuthis was ~1.7 m. These encounters suggest that unobtrusive camera platforms with luminescent lures are effective tools for attracting and studying large deep-sea squids.

Summary Transparent zooplankton and nekton are often nearly invisible when viewed under ambient light in the pelagic zone [1–3]. However, in this environment, where the light field is directional (and thus likely to cause reflections), and under the bioluminescent searchlights of potential predators, animals may be revealed by reflections from their body surface [4–7]. We investigated the cuticle surfaces of seven species of hyperiids (Crustacea; Amphipoda) using scanning electron microscopy and found two undocumented features that may reduce reflectance. We found that the legs of Cystisoma spp. (n = 5) are covered with an ordered array of nanoprotuberances 200 ± 20 nm SD in height that function optically as a gradient refractive index material [6, 8, 9]. Additionally, we observed that Cystisoma and six other species of hyperiids are covered with a monolayer of homogenous spheres (diameters ranging from 52 ± 7 nm SD on Cystisoma spp. to 320 ± 15 nm SD on Phronima spp.). Optical modeling using effective medium theory and transfer matrix methods demonstrated that both the nanoprotuberances and the monolayers reduce reflectance by as much as 100-fold, depending on the wavelength and angle of the incident light and the thickness of the gradient layer. Even though we only consider surface reflectance and not internal light scattering, our study demonstrates that these nanoprotuberances and spheres can improve crypsis in a featureless habitat where the smallest reflection can render an animal vulnerable to visual predation.

This is a pre-copyedited, author-produced version of an article accepted for publication in Integrative & Comparative Biology following peer review. The version of record Thomas W. Cronin, Sönke Johnsen; Extraocular, Non-Visual, and Simple Photoreceptors: An Introduction to the Symposium, Integrative and Comparative Biology, Volume 56, Issue 5, 1 November 2016, Pages 758–763, https://doi.org/10.1093/icb/icw106 is available online at: https://doi.org/10.1093/icb/icw106 or https://academic.oup.com/icb/article/56/5/758/2420636., It has been recognized for decades that animals sense light using photoreceptors besides those that are devoted strictly to vision. However, the nature of these receptors, their molecular components, their physiological responses, and their biological functions are often obscure. Only recently have researchers begun to learn how critical these non-visual or very simple visual responses are to organismal function; and new approaches, including high-throughput molecular genetic techniques, have led to a revolution in our understanding of the evolution, anatomical distribution, physiology, and – in some cases – function of non-visual photoreception in a diverse assemblage of organisms. Historically, these types of receptors have been described primarily among invertebrates, although they were recognized to be present in fishes, reptiles, and birds. Their presence in mammals was completely unsuspected until the end of the 20th century. In the following papers, we bring together specialists from throughout the field to review the current state of knowledge regarding extraocular, non-visual, and simple photoreceptors in a large diversity of organisms ranging from protists to advanced vertebrates and invertebrates.

The eyes of scallops form images using a concave spherical mirror and contain two separate retinas, one layered on top of the other. Behavioral and electrophysiological studies indicate that the images formed by these eyes have angular resolutions of about 2°. Based on previous ray-tracing models, it has been thought that the more distal of the two retinas lies near the focal point of the mirror and that the proximal retina, positioned closer to the mirror at the back of the eye, receives light that is out-of-focus. Here, we propose three mechanisms through which both retinas may receive focused light: (1) chromatic aberration produced by the lens may cause the focal points for longer and shorter wavelengths to fall near the distal and proximal retinas, respectively; (2) focused light from near and far objects may fall on the distal and proximal retinas, respectively; and (3) the eyes of scallops may be dynamic structures that change shape to determine which retina receives focused light. To test our hypotheses, we used optical coherence tomography (OCT), a method of near-infrared optical depth-ranging, to acquire virtual cross-sections of live, intact eyes from the bay scallop Argopecten irradians . Next, we used a custom-built ray-tracing model to estimate the qualities of the images that fall on an eye’s distal and proximal retinas as functions of the wavelengths of light entering the eye (400–700 nm), object distances (0.01–1 m), and the overall shape of the eye. When we assume 550 nm wavelength light and object distances greater than 0.01 m, our model predicts that the angular resolutions of the distal and proximal retinas are 2° and 7°, respectively. Our model also predicts that neither chromatic aberration nor differences in object distance lead to focused light falling on the distal and proximal retinas simultaneously. However, if scallops can manipulate the shapes of their eyes, perhaps through muscle contractions, we speculate that they may be able to influence the qualities of the images that fall on their proximal retinas and—to a lesser extent—those that fall on their distal retinas as well.

RGB displays effectively simulate millions of colors in the eyes of humans by modulating the relative amount of light emitted by 3 differently colored juxtaposed lights (red, green, and blue). The relationship between the ratio of red, green, and blue light and the perceptual experience of that light has been well defined by psychophysical experiments in humans, but is unknown in animals. The perceptual experience of an animal looking at an RGB display of imagery designed for humans is likely to poorly represent an animal’s experience of the same stimulus in the real world. This is due, in part, to the fact that many animals have different numbers of photoreceptor classes than humans do and that their photoreceptor classes have peak sensitivities centered over different parts of the ultraviolet and visible spectrum. However, it is sometimes possible to generate videos that accurately mimic natural stimuli in the eyes of another animal, even if that animal’s sensitivity extends into the ultraviolet portion of the spectrum. How independently each RGB phosphor stimulates each of an animal’s photoreceptor classes determines the range of colors that can be simulated for that animal. What is required to determine optimal color rendering for another animal is a device capable of measuring absolute or relative quanta of light across the portion of the spectrum visible to the animal (i.e., a spectrometer), and data on the spectral sensitivities of the animal’s photoreceptor classes. In this article, we outline how to use such equipment and information to generate video stimuli that mimic, as closely as possible, an animal’s color perceptual experience of real-world objects. Key words: color vision, computer animation, perception, video playback, virtual reality.

The measurement of color in biology has become increasingly common. These measurements are not limited to color vision research, but are also found in studies of communication, signaling, camouflage, evolution and behavior, and in the examination of environmental, artificial and biogenic light. Although the recent availability of portable spectrometers has made it simpler to measure color, guidance on how to make these measurements has not kept pace. Because most biologists receive little training in optics, many measure the wrong thing, or measure the right thing in the wrong way. This Commentary attempts to give biologists a brief overview of how to measure light and color using spectrometers and calibrated photographs. It focuses in particular on the inherent ambiguities of many optical measurements, and how these can be addressed.

Magnetoreception remains one of the most enigmatic of animal senses. Rainbow trout (Oncorhynchus mykiss) represent an ideal species to study this sense, as magnetoreception based upon microscopic particles of magnetite is suspected to play an important role in their orientation and navigation. Here we found that compared with controls, a magnetic pulse (a treatment commonly used to demonstrate magnetite-based magnetoreception) can induce orientation behavior in juvenile rainbow trout on a specific experimental day. Multiple circular-linear regression also indicated that this effect could at least be partially explained by daily variation in solar electromagnetic activity (i.e., sunspot count and disturbance storm time index). These results are consistent with magnetite-based magnetoreception in rainbow trout and suggest that 1) solar activity may impact magnetic orientation and 2) researchers should be cognizant of its potential consequences on studies of magnetoreception.

For polarized light to inform behaviour, the typical range of degrees of polarization observable in the animal’s natural environment must be above the threshold for detection and interpretation. Here we present the first investigation of the degree of linear polarization threshold for orientation behaviour in a nocturnal species, with specific reference to the range of degrees of polarization measured in the night sky. An effect of lunar phase on the degree of polarization of skylight was found, with smaller illuminated fractions of the moon’s surface corresponding to lower degrees of polarization in the night sky. We found that South African dung beetleEscarabaeus satyrus(Boheman, 1860) can orient to polarized light for a range of degrees of polarization similar to that observed in diurnal insects, reaching a lower threshold between 0.04 and 0.32, possibly as low as 0.11. For degrees of polarization lower than 0.23, as measured on a crescent moon night, orientation performance was considerably weaker than that observed for completely linearly-polarized stimuli, but was nonetheless stronger than in the absence of polarized light.Summary StatementA degree-of-polarization threshold for orientation behaviour is reported for nocturnal dung beetleEscarabaeus satyrusin the context of measurements showing changes in the degree of polarization of skylight with lunar phase.

Like many birds [1], numerous species of nocturnal moths undertake spectacular long-distance migrations at night [2]. Each spring, billions of Bogong moths (Agrotis infusa) escape hot conditions in different regions of southeast Australia by making a highly directed migration of over 1,000 km to a limited number of cool caves in the Australian Alps, historically used for aestivating over the summer [3, 4]. How moths determine the direction of inherited migratory trajectories at night and locate their destination (i.e., navigate) is currently unknown [5–7]. Here we show that Bogong moths can sense the Earth's magnetic field and use it in conjunction with visual landmarks to steer migratory flight behavior. By tethering migrating moths in an outdoor flight simulator [8], we found that their flight direction turned predictably when dominant visual landmarks and a natural Earth-strength magnetic field were turned together, but that the moths became disoriented within a few minutes when these cues were set in conflict. We thus conclude that Bogong moths, like nocturnally migrating birds [9], can use a magnetic sense. Our results represent the first reliable demonstration of the use of the Earth's magnetic field to steer flight behavior in a nocturnal migratory insect. The nocturnal Bogong moth performs a highly directed long-distance migration to and from alpine caves in the Australian Alps. Dreyer et al. show that this moth senses the Earth's magnetic field and uses it together with visual landmarks to steer migratory flight behavior. The geomagnetic field might thus be used as a compass during migration. (Less)

Cleaner shrimp and their reef fish clients are an interspecific mutualistic interaction that is thought to be mediated by signals, and a useful system for studying the dynamics of interspecific signalling. To demonstrate signalling, one must show that purported signals at minimum (a) result in a consistent state change in the receiver and (b) contain reliable information about the sender's intrinsic state or future behaviour. Additionally, signals must be perceptible by receivers. Here, we document fundamental attributes of the signalling system between the cleaner shrimp Ancylomenes pedersoni and its clients. First, we use sequential analysis of in situ behavioural interactions to show that cleaner antenna whipping reliably predicts subsequent cleaning. If shrimp do not signal via antenna whipping, clients triple their likelihood of being cleaned by adopting darker coloration over a matter of seconds, consistent with dark colour change signalling that clients want cleaning. Using experimental manipulations, we found that visual stimuli are sufficient to elicit antenna whipping, and that shrimp are more likely to ‘clean' dark than light visual stimuli. Lastly, we show that antenna whipping and colour change are perceptible when accounting for the intended receiver's visual acuity and spectral sensitivity, which differ markedly between cleaners and clients. Our results show that signalling by both cleaners and clients can initiate and mediate their mutualistic interaction.

The iconic red hourglass of the black widow spiders (genus Latrodectus) is traditionally considered an aposematic signal, yet experimental evidence is lacking. Here, we present data that suggest that black widow coloration may have evolved to be an aposematic signal that is more conspicuous to their vertebrate predators than to their insect prey. In choice experiments with wild birds, we found that the red-and-black coloration deters potential predators: Wild birds were ~3 times less likely to attack a black widow model with an hourglass than one without. Using visual-system appropriate models, we also found that a black widow’s red-and-black color combo is more apparent to a typical bird than a typical insect. Additionally, an ancestral reconstruction reveals that red dorsal coloration is ancestral in black widows and that at some point some North American widows lost their red dorsal coloration. Behaviorally, differences in red dorsal coloration between 2 North American species are accompanied by differences in microhabitat that affects how often a bird will view a black widow’s dorsal region. All observations are consistent with a cost–benefit trade-off of being more conspicuous to predators than to prey. We suggest that limiting detection by prey may help explain why red and black aposematic signals occur frequently in nature.

Summary The mesopelagic habitat is a vast space that lacks physical landmarks and is structured by depth, light penetration, and horizontal currents. Solar illumination is visible in the upper 1,000 m of the ocean, becoming dimmer and spectrally filtered with depth—generating a nearly monochromatic blue light field [1]. The struggle to perceive dim downwelling light and bioluminescent sources and the need to remain unseen generate contrasting selective pressures on the eyes of mesopelagic inhabitants [2]. Hyperiid amphipods are cosmopolitan members of the mesopelagic fauna with at least ten different eye configurations across the family—ranging from absent eyes in deep-living species to four enlarged eyes in mesopelagic individuals [3–7]. The hyperiid amphipod Paraphronima gracilis has a pair of bi-lobed apposition compound eyes, each with a large upward-looking portion and a small lateral-looking portion. The most unusual feature of the P. gracilis eye is that its upward-looking portion is resolved into a discontinuous retina with 12 distinct groups, each serving one transverse row of continuously spaced facets. On the basis of eye morphology, we estimated spatial acuity (2.5° ± 0.11°, SEM; n = 25) and optical sensitivity (30 ± 3.4 μm 2 ⋅ sr, SEM; n = 25). Microspectrophotometry showed that spectral sensitivity of the eye peaked at 516 nm (±3.9 nm, SEM; n = 6), significantly offset from the peak of downwelling irradiance in the mesopelagic realm (480 nm). Modeling of spatial summation within the linear retinal groups showed that it boosts sensitivity with less cost to spatial acuity than more typical configurations.

A wide variety of marine animals, including animals as different as cephalopods, echinoderms and fish, use suction adhesion for temporary or long-term attachments (1). One aspect of suction adhesion that has been discussed, but never tested experimentally, is its dependence on depth. The change in hydrostatic pressure with depth may exert a marked effect on the force of attachment produced by suction (2-6). This study was designed to confirm this effect experimentally, using limpets as a test case. Limpets rely on suction to resist dislodgment by predators and crashing waves (7, 8). We measured the suction tenacity of four species of limpets at sea level and at increased ambient pressure in a hyperbaric chamber. Tenacity is defined as the force of attachment divided by the area of the foot contacting the substratum. Change in ambient pressure had a small but significant effect on limpet tenacity. These results show that depth can affect attachment up to a point, but the mechanics of limpet feet appear incapable of producing dramatically larger tenacities. Increasing hydrostatic pressure raises the upper limit on the force of attachment that a sucker can create (5). This can be explained as follows. A sucker forms an attachment by decreasing the pressure of the water it encloses. This results in a differential between the pressure of the water outside the sucker and the pressure inside. This differential pulls the sucker against the substratum. The pressure outside the sucker is the ambient pressure, which increases by 100 kPa (1 atm) with each 0-m depth increase. The minimum pressure inside the sucker is limited by water's tensile strength. The sucker can reduce the pressure until the tension in the water reaches a critical value, at which point the water cavitates; it undergoes

A major goal of sensory ecology is to identify factors that underlie sensory-trait variation. One open question centers on why fishes show the greatest diversity among vertebrates in their capacity to detect color (i.e., spectral sensitivity). Over the past several decades, λmax values (photoreceptor class peak sensitivity) and chromacy (photoreceptor class number) have been cataloged for hundreds of fish species, yet the ecological basis of this diversity and the functional significance of high chromacy levels (e.g., tetra- and pentachromacy) remain unclear. In this study, we examined phylogenetic, physiological, and ecological patterns of spectral sensitivity of ray-finned fishes (Actinoptergyii) via a meta-analysis of data compiled from 213 species. Across the fishes sampled, our results indicate that trichromacy is most common, ultraviolet λmax values are not found in monochromatic or dichromatic species, and increasing chromacy, including from tetra- to pentachromacy, significantly increases spectral sensitivity range. In an ecological analysis, multivariate phylogenetic latent liability modeling was performed to analyze correlations between chromacy and five hypothesized predictors (depth, habitat, diet, body coloration, and body size). In a model not accounting for phylogenetic relatedness, each predictor with the exception of habitat significantly correlated with chromacy: a positive relationship in body color and negative relationships with body size, diet, and depth. However, after phylogenetic correction, the only remaining correlated predictor was depth. The findings of this study indicate that phyletic heritage and depth are important factors in fish spectral sensitivity and impart caution about excluding phylogenetic comparative methods in studies of sensory trait variation.

Whole-body transparency, an effective camouflage strategy in many aquatic species, can be disrupted by environmental and/or physiological stressors. We found that tail-flip escape responses temporarily disrupt the transparency of the anemone shrimp

Diverse animals use Earth's magnetic field in orientation and navigation, but little is known about the molecular mechanisms that underlie magnetoreception. Recent studies have focused on two possibilities: (i) magnetite-based receptors; and (ii) biochemical reactions involving radical pairs. We used RNA sequencing to examine gene expression in the brain of rainbow trout (Oncorhynchus mykiss) after exposure to a magnetic pulse known to disrupt magnetic orientation behaviour. We identified 181 differentially expressed genes, including increased expression of six copies of the frim gene, which encodes a subunit of the universal iron-binding and trafficking protein ferritin. Functions linked to the oxidative effects of free iron (e.g. oxidoreductase activity, transition metal ion binding, mitochondrial oxidative phosphorylation) were also affected. These results are consistent with the hypothesis that a magnetic pulse alters or damages magnetite-based receptors and/or other iron-containing structures, which are subsequently repaired or replaced through processes involving ferritin. Additionally, some genes that function in the development and repair of photoreceptive structures (e.g. crggm3, purp, prl, gcip, crabp1 and pax6) were also differentially expressed, raising the possibility that a magnetic pulse might affect structures and processes unrelated to magnetite-based magnetoreceptors.

Many pelagic species, particularly teleost fish, have silvered lateral surfaces that are thought to primarily serve as a form of camouflage. The underlying argument is that the underwater light field is cylindrically symmetrical around the vertical axis; thus a vertical mirror reflects a region of the water column that matches the region directly behind the mirror. However, the degree of symmetry of the underwater light field itself has not been assessed. Modeled underwater radiances from the surface to a depth of 100 m using measured profiles of inherent optical properties and HydroLight radiative transfer software showed that the horizontal light field under sunny conditions was asymmetrical over a wide range of solar elevations. In addition, the maximum asymmetry at 100 m occurred not when the sun was near the horizon, but when it was 45u above it. We validated these modeled results in Hawaiian waters using a modification of a commercial radiometer. Both modeled and measured radiances showed that the inherent contrast of silvery fish was typically higher at longer wavelengths. However, models of the sighting distances of these surfaces showed that sighting distance was greatest at the peak wavelength of the downwelling irradiance (,480 nm). The modeled and measured asymmetry of the horizontal light field implies that mirror camouflage is not always as successful as originally thought and suggests that there may be further refinements for this form of crypsis that have not been previously considered.

The bay scallopArgopecten irradians(Mollusca: Bivalvia) has dozens of iridescent blue eyes that focus light using mirror-based optics. Here, we test the hypothesis that these eyes appear blue because of photonic nanostructures that preferentially scatter short-wavelength light. Using transmission electron microscopy, we found that the epithelial cells covering the eyes ofA. irradianshave three distinct layers: an outer layer of microvilli, a middle layer of random close-packed nanospheres and an inner layer of pigment granules. The nanospheres are approximately 180 nm in diameter and consist of electron-dense cores approximately 140 nm in diameter surrounded by less electron-dense shells 20 nm thick. They are packed at a volume density of approximately 60% and energy-dispersive X-ray spectroscopy indicates that they are not mineralized. Optical modelling revealed that the nanospheres are an ideal size for producing angle-weighted scattering that is bright and blue. A comparative perspective supports our hypothesis: epithelial cells from the black eyes of the sea scallopPlacopecten magellanicushave an outer layer of microvilli and an inner layer of pigment granules but lack a layer of nanospheres between them. We speculate that light-scattering nanospheres help to prevent UV wavelengths from damaging the internal structures of the eyes ofA. irradiansand other blue-eyed scallops.