Program in Sensory Physiology and Behavior
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The Program in Sensory Physiology and Behavior, Marine Biological Laboratory focuses on research in vision, balance and hearing. Researchers use marine or aquatic model organisms (cephalopods, fishes, turtles) to take advantage of the unique seawater facilities and the microscopy and imaging centers at the MBL.
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ArticleOctopus arms exhibit exceptional flexibility(Nature Research, 2020-11-30)The octopus arm is often referred to as one of the most flexible limbs in nature, yet this assumption requires detailed inspection given that this has not been measured comprehensively for all portions of each arm. We investigated the diversity of arm deformations in Octopus bimaculoides with a frame-by-frame observational analysis of laboratory video footage in which animals were challenged with different tasks. Diverse movements in these hydrostatic arms are produced by some combination of four basic deformations: bending (orally, aborally; inward, outward), torsion (clockwise, counter-clockwise), elongation, and shortening. More than 16,500 arm deformations were observed in 120 min of video. Results showed that all eight arms were capable of all four types of deformation along their lengths and in all directions. Arms function primarily to bring the sucker-lined oral surface in contact with target surfaces. Bending was the most common deformation observed, although the proximal third of the arms performed relatively less bending and more shortening and elongation as compared with other arm regions. These findings demonstrate the exceptional flexibility of the octopus arm and provide a basis for investigating motor control of the entire arm, which may aid the future development of soft robotics.
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ArticleMale alternative reproductive tactics and associated evolution of anatomical characteristics in loliginid squid(Frontiers Media, 2019-10-15)Loliginid squids provide a unique model system to explore male alternative reproductive tactics (ARTs) and their linkage to size, behavioral decision making, and possibly age. Large individuals fight one another and the winners form temporary consortships with females, while smaller individuals do not engage in male-male agonistic bouts but use various sneaker tactics to obtain matings, each with varying mating and fertilization success. There is substantial behavioral flexibility in most species, as smaller males can facultatively switch to the alternative consort behaviors as the behavioral context changes. These forms of ARTs can involve different: mating posture; site of spermatophore deposition; fertilization success; and sperm traits. Most of the traits of male dimorphism (both anatomical and behavioral) are consistent with traditional sexual selection theory, while others have unique features that may have evolved in response to the fertilization environment faced by each temporary or permanent male morph.
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ArticleLateralization of eye use in cuttlefish : opposite direction for anti-predatory and predatory behaviors(Frontiers Media, 2016-12-12)Vertebrates with laterally placed eyes typically exhibit preferential eye use for ecological activities such as scanning for predators or prey. Processing visual information predominately through the left or right visual field has been associated with specialized function of the left and right brain. Lateralized vertebrates often share a general pattern of lateralized brain function at the population level, whereby the left hemisphere controls routine behaviors and the right hemisphere controls emergency responses. Recent studies have shown evidence of preferential eye use in some invertebrates, but whether the visual fields are predominately associated with specific ecological activities remains untested. We used the European common cuttlefish, Sepia officinalis, to investigate whether the visual field they use is the same, or different, during anti-predatory, and predatory behavior. To test for lateralization of anti-predatory behavior, individual cuttlefish were placed in a new environment with opaque walls, thereby obliging them to choose which eye to orient away from the opaque wall to scan for potential predators (i.e., vigilant scanning). To test for lateralization of predatory behavior, individual cuttlefish were placed in the apex of an isosceles triangular arena and presented with two shrimp in opposite vertexes, thus requiring the cuttlefish to choose between attacking a prey item to the left or to the right of them. Cuttlefish were significantly more likely to favor the left visual field to scan for potential predators and the right visual field for prey attack. Moreover, individual cuttlefish that were leftward directed for vigilant scanning were predominately rightward directed for prey attack. Lateralized individuals also showed faster decision-making when presented with prey simultaneously. Cuttlefish appear to have opposite directions of lateralization for anti-predatory and predatory behavior, suggesting that there is functional specialization of each optic lobe (i.e., brain structures implicated in visual processing). These results are discussed in relation to the role of lateralized brain function and the evolution of population level lateralization.
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Book chapterA brief review of cephalopod behavioral responses to sound( 2016)Sound is a widely available cue in aquatic environments and is used by many marine animals for vital behaviors. Most research has focused on marine vertebrates. Relatively little is known about sound detection in marine invertebrates despite their abundance and importance in marine environments. Cephalopods are a key taxon in many ecosystems but their behavioral interactions relative to acoustic stimuli have seldom been studied. Here we review current knowledge regarding (i) frequency ranges and sound levels that generate behavioral responses, (ii) the types of behavioral responses and their biological relevance.
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ArticleTactical decisions for changeable cuttlefish camouflage : visual cues for choosing masquerade are relevant from a greater distance than visual cues used for background matching(Marine Biological Laboratory, 2015-10-01)Cuttlefish use multiple camouflage tactics to evade their predators. Two common tactics are background matching (resembling the background to hinder detection) and masquerade (resembling an uninteresting or inanimate object to impede detection or recognition). We investigated how the distance and orientation of visual stimuli affected the choice of these two camouflage tactics. In the current experiments, cuttlefish were presented with three visual cues: 2D horizontal floor, 2D vertical wall, and 3D object. Each was placed at several distances: directly beneath (in a circle whose diameter was one body length (BL); at zero BL [(0BL); i.e., directly beside, but not beneath the cuttlefish]; at 1BL; and at 2BL. Cuttlefish continued to respond to 3D visual cues from a greater distance than to a horizontal or vertical stimulus. It appears that background matching is chosen when visual cues are relevant only in the immediate benthic surroundings. However, for masquerade, objects located multiple body lengths away remained relevant for choice of camouflage.
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ArticleThe killer fly hunger games : target size and speed predict decision to pursuit(S. Karger AG, Basel, 2015-09-24)Predatory animals have evolved to optimally detect their prey using exquisite sensory systems such as vision, olfaction and hearing. It may not be so surprising that vertebrates, with large central nervous systems, excel at predatory behaviors. More striking is the fact that many tiny insects, with their miniscule brains and scaled down nerve cords, are also ferocious, highly successful predators. For predation, it is important to determine whether a prey is suitable before initiating pursuit. This is paramount since pursuing a prey that is too large to capture, subdue or dispatch will generate a substantial metabolic cost (in the form of muscle output) without any chance of metabolic gain (in the form of food). In addition, during all pursuits, the predator breaks its potential camouflage and thus runs the risk of becoming prey itself. Many insects use their eyes to initially detect and subsequently pursue prey. Dragonflies, which are extremely efficient predators, therefore have huge eyes with relatively high spatial resolution that allow efficient prey size estimation before initiating pursuit. However, much smaller insects, such as killer flies, also visualize and successfully pursue prey. This is an impressive behavior since the small size of the killer fly naturally limits the neural capacity and also the spatial resolution provided by the compound eye. Despite this, we here show that killer flies efficiently pursue natural (Drosophila melanogaster) and artificial (beads) prey. The natural pursuits are initiated at a distance of 7.9 ± 2.9 cm, which we show is too far away to allow for distance estimation using binocular disparities. Moreover, we show that rather than estimating absolute prey size prior to launching the attack, as dragonflies do, killer flies attack with high probability when the ratio of the prey's subtended retinal velocity and retinal size is 0.37. We also show that killer flies will respond to a stimulus of an angular size that is smaller than that of the photoreceptor acceptance angle, and that the predatory response is strongly modulated by the metabolic state. Our data thus provide an exciting example of a loosely designed matched filter to Drosophila, but one which will still generate successful pursuits of other suitable prey.
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ArticleAn unexpected diversity of photoreceptor classes in the longfin squid, Doryteuthis pealeii(Public Library of Science, 2015-09-09)Cephalopods are famous for their ability to change color and pattern rapidly for signaling and camouflage. They have keen eyes and remarkable vision, made possible by photoreceptors in their retinas. External to the eyes, photoreceptors also exist in parolfactory vesicles and some light organs, where they function using a rhodopsin protein that is identical to that expressed in the retina. Furthermore, dermal chromatophore organs contain rhodopsin and other components of phototransduction (including retinochrome, a photoisomerase first found in the retina), suggesting that they are photoreceptive. In this study, we used a modified whole-mount immunohistochemical technique to explore rhodopsin and retinochrome expression in a number of tissues and organs in the longfin squid, Doryteuthis pealeii. We found that fin central muscles, hair cells (epithelial primary sensory neurons), arm axial ganglia, and sucker peduncle nerves all express rhodopsin and retinochrome proteins. Our findings indicate that these animals possess an unexpected diversity of extraocular photoreceptors and suggest that extraocular photoreception using visual opsins and visual phototransduction machinery is far more widespread throughout cephalopod tissues than previously recognized.
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PreprintGiant Australian cuttlefish use mutual assessment to resolve male-male contests( 2015-05)Game theory models provide a useful framework for investigating strategies of conflict resolution in animal contests. Model predictions are based on estimates of resource-holding potential (RHP) and vary in their assumptions about how opponents gather information about RHP. Models can be divided into self-assessment strategies (energetic war-of-attrition, E-WOA; cumulative assessment model, CAM) and mutual assessment strategies (sequential assessment model, SAM). We used laboratory-staged contests between male giant Australian cuttlefish, Sepia apama, to evaluate RHP traits and to test game theory models. Mantle length was a key indicator of RHP because it predicted contest outcome, whereby larger individuals were more likely to win a contest. Winners and losers did not match behaviours, ruling out the E-WOA. There was no relationship between contest outcome, duration and escalation rates, arguing against the CAM. Persistence to continue a contest was based on RHP asymmetry, rather than loser and/or winner RHP, providing support for the SAM. Motivation to fight was determined from a male’s latency to resume a contest following the introduction of a female during a contest. The latency to resume a contest was negatively related to the size of the focal male and positively related to the size of their opponent. These results show that competing males are able to gather information concerning RHP asymmetries, providing support for mutual assessment. Furthermore, males showed significant behavioural differences in their responses to relatively larger than to relatively smaller opponents. Using an integrative approach, our study provides a well-substantiated example of mutual assessment.
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PreprintVisual phototransduction components in cephalopod chromatophores suggest dermal photoreception( 2015-04)Cephalopod molluscs are renowned for their colorful and dynamic body patterns, produced by an assemblage of skin components that interact with light. These may include iridophores, leucophores, chromatophores, and (in some species) photophores. Here, we present molecular evidence suggesting that cephalopod chromatophores, small dermal pigmentary organs that reflect various colors of light, are photosensitive. RT-PCR revealed the presence of transcripts encoding rhodopsin and retinochrome within the retinas and skin of the squid Doryteuthis pealeii, and the cuttlefish Sepia officinalis and Sepia latimanus. In D. pealeii, Gqα and squid TRP channel transcripts were present in the retina and in all dermal samples. Rhodopsin, retinochrome, and Gqα transcripts were also found in RNA extracts from dissociated chromatophores isolated from D. pealeii dermal tissues. In D. pealeii, immunohistochemical staining labeled rhodopsin, retinochrome, and Gqα proteins in several chromatophore components, including pigment cell membranes, radial muscle fibers, and sheath cells. This is the first evidence that cephalopod dermal tissues, and specifically chromatophores, may possess the requisite combination of molecules required to respond to light.
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ArticleVirtual finger boosts three-dimensional imaging and microsurgery as well as terabyte volume image visualization and analysis(Nature Publishing Group, 2014-07-11)Three-dimensional (3D) bioimaging, visualization and data analysis are in strong need of powerful 3D exploration techniques. We develop virtual finger (VF) to generate 3D curves, points and regions-of-interest in the 3D space of a volumetric image with a single finger operation, such as a computer mouse stroke, or click or zoom from the 2D-projection plane of an image as visualized with a computer. VF provides efficient methods for acquisition, visualization and analysis of 3D images for roundworm, fruitfly, dragonfly, mouse, rat and human. Specifically, VF enables instant 3D optical zoom-in imaging, 3D free-form optical microsurgery, and 3D visualization and annotation of terabytes of whole-brain image volumes. VF also leads to orders of magnitude better efficiency of automated 3D reconstruction of neurons and similar biostructures over our previous systems. We use VF to generate from images of 1,107 Drosophila GAL4 lines a projectome of a Drosophila brain.
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ArticleUse of spectroscopy for assessment of color discrimination in animal vision(Optical Society, 2013-12-19)Animals use color vision for a number of tasks including food localization, object recognition, communication, and mate selection. For these and other specific behaviors involving the use of color cues, models that quantify color discriminability have been developed. These models take as input the photoreceptor spectral sensitivities of the animal and radiance spectra of the surfaces of interest. These spectra are usually acquired using spectroscopic instruments that collect point-by-point data and can easily yield signals contaminated with neighboring colors if not operated carefully. In this paper, I present an equation that relates the optical fiber diameter and numerical aperture to the measurement angle and distance needed to record uncontaminated spectra. I demonstrate its utility by testing the discriminability of two solid colors for the visual systems of a dichromatic ferret and a trichromatic frog in (1) a conspicuous scenario where the colors have little spectral overlap and (2) a perfect camouflage scenario where the spectra are identical. This equation is derived from geometrical optics and is applicable to spectroscopic measurements in all fields.
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PreprintExpression of squid iridescence depends on environmental luminance and peripheral ganglion control( 2013-10)Squids display impressive changes in body coloration that are afforded by two types of dynamic skin elements: structural iridophores (which produce iridescence) and pigmented chromatophores. Both color elements are neurally controlled, but nothing is known about the iridescence circuit, or the environmental cues, that elicit iridescence expression. To tackle this knowledge gap, we performed denervation, electrical stimulation and behavioral experiments using the long-fin squid, Doryteuthis pealeii. We show that while the pigmentary and iridescence circuits originate in the brain, they are wired differently in the periphery: (i) the iridescence signals are routed through a peripheral center called the stellate ganglion and (ii) the iridescence motorneurons likely originate within this ganglion (as revealed by nerve fluorescence dye fills). Cutting the inputs to the stellate ganglion that descend from the brain shifts highly reflective iridophores into a transparent state. Taken together, these findings suggest that although brain commands are necessary for expression of iridescence, integration with peripheral information in the stellate ganglion could modulate the final output. We also demonstrate that squids change their iridescence brightness in response to environmental luminance; such changes are robust but slow (minutes to hours). The squid's ability to alter its iridescence levels may improve camouflage under different lighting intensities.
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ArticleUse of commercial off-the-shelf digital cameras for scientific data acquisition and scene-specific color calibration(Optical Society of America, 2014-01-20)Commercial off-the-shelf digital cameras are inexpensive and easy-to-use instruments that can be used for quantitative scientific data acquisition if images are captured in raw format and processed so that they maintain a linear relationship with scene radiance. Here we describe the image-processing steps required for consistent data acquisition with color cameras. In addition, we present a method for scene-specific color calibration that increases the accuracy of color capture when a scene contains colors that are not well represented in the gamut of a standard color-calibration target. We demonstrate applications of the proposed methodology in the fields of biomedical engineering, artwork photography, perception science, marine biology, and underwater imaging.
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ArticleDefensive responses of cuttlefish to different teleost predators(Marine Biological Laboratory, 2013-12-01)We evaluated cuttlefish (Sepia officinalis) responses to three teleost predators: bluefish (Pomatomus saltatrix), summer flounder (Paralichthys dentatus), and black seabass (Centropristis striata). We hypothesized that the distinct body shapes, swimming behaviors, and predation tactics exhibited by the three fishes would elicit markedly different antipredator responses by cuttlefish. Over the course of 25 predator-prey behavioral trials, 3 primary and 15 secondary defense behaviors of cuttlefish were shown to predators. In contrast, secondary defenses were not shown during control trials in which predators were absent. With seabass—a benthic, sit-and-pursue predator—cuttlefish used flight and spent more time swimming in the water column than with other predators. With bluefish—an active, pelagic searching predator—cuttlefish remained closely associated with the substrate and relied more on cryptic behaviors. Startle (deimatic) displays were the most frequent secondary defense shown to seabass and bluefish, particularly the Dark eye ring and Deimatic spot displays. We were unable to evaluate secondary defenses by cuttlefish to flounder—a lie-and-wait predator—because flounder did not pursue cuttlefish or make attacks. Nonetheless, cuttlefish used primary defense during flounder trials, alternating between cryptic still and moving behaviors. Overall, our results suggest that cuttlefish may vary their behavior in the presence of different teleost predators: cryptic behaviors may be more important in the presence of active searching predators (e.g., bluefish), while conspicuous movements such as swimming in the water column and startle displays may be more prevalent with relatively sedentary, bottom-associated predators (e.g., seabass).
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ArticleThe giant eyes of giant squid are indeed unexpectedly large, but not if used for spotting sperm whales(BioMed Central, 2013-09-08)We recently reported (Curr Biol 22:683–688, 2012) that the eyes of giant and colossal squid can grow to three times the diameter of the eyes of any other animal, including large fishes and whales. As an explanation to this extreme absolute eye size, we developed a theory for visual performance in aquatic habitats, leading to the conclusion that the huge eyes of giant and colossal squid are uniquely suited for detection of sperm whales, which are important squid-predators in the depths where these squid live. A paper in this journal by Schmitz et al. (BMC Evol Biol 13:45, 2013) refutes our conclusions on the basis of two claims: (1) using allometric data they argue that the eyes of giant and colossal squid are not unexpectedly large for the size of the squid, and (2) a revision of the values used for modelling indicates that large eyes are not better for detection of approaching sperm whales than they are for any other task. We agree with Schmitz et al. that their revised values for intensity and abundance of planktonic bioluminescence may be more realistic, or at least more appropriately conservative, but argue that their conclusions are incorrect because they have not considered some of the main arguments put forward in our paper. We also present new modelling to demonstrate that our conclusions remain robust, even with the revised input values suggested by Schmitz et al.
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ArticleSquid have nociceptors that display widespread long-term sensitization and spontaneous activity after bodily injury(Society for Neuroscience, 2013-06-12)Bodily injury in mammals often produces persistent pain that is driven at least in part by long-lasting sensitization and spontaneous activity (SA) in peripheral branches of primary nociceptors near sites of injury. While nociceptors have been described in lower vertebrates and invertebrates, outside of mammals there is limited evidence for peripheral sensitization of primary afferent neurons, and there are no reports of persistent SA being induced in primary afferents by noxious stimulation. Cephalopod molluscs are the most neurally and behaviorally complex invertebrates, with brains rivaling those of some vertebrates in size and complexity. This has fostered the opinion that cephalopods may experience pain, leading some governments to include cephalopods under animal welfare laws. It is not known, however, if cephalopods possess nociceptors, or whether their somatic sensory neurons exhibit nociceptive sensitization. We demonstrate that squid possess nociceptors that selectively encode noxious mechanical but not heat stimuli, and that show long-lasting peripheral sensitization to mechanical stimuli after minor injury to the body. As in mammals, injury in squid can cause persistent SA in peripheral afferents. Unlike mammals, the afferent sensitization and SA are almost as prominent on the contralateral side of the body as they are near an injury. Thus, while squid exhibit peripheral alterations in afferent neurons similar to those that drive persistent pain in mammals, robust changes far from sites of injury in squid suggest that persistently enhanced afferent activity provides much less information about the location of an injury in cephalopods than it does in mammals.
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ArticleVertical visual features have a strong influence on cuttlefish camouflage(Marine Biological Laboratory, 2013-04)Cuttlefish and other cephalopods use visual cues from their surroundings to adaptively change their body pattern for camouflage. Numerous previous experiments have demonstrated the influence of two-dimensional (2D) substrates (e.g., sand and gravel habitats) on camouflage, yet many marine habitats have varied three-dimensional (3D) structures among which cuttlefish camouflage from predators, including benthic predators that view cuttlefish horizontally against such 3D backgrounds. We conducted laboratory experiments, using Sepia officinalis, to test the relative influence of horizontal versus vertical visual cues on cuttlefish camouflage: 2D patterns on benthic substrates were tested versus 2D wall patterns and 3D objects with patterns. Specifically, we investigated the influence of (i) quantity and (ii) placement of high-contrast elements on a 3D object or a 2D wall, as well as (iii) the diameter and (iv) number of 3D objects with high-contrast elements on cuttlefish body pattern expression. Additionally, we tested the influence of high-contrast visual stimuli covering the entire 2D benthic substrate versus the entire 2D wall. In all experiments, visual cues presented in the vertical plane evoked the strongest body pattern response in cuttlefish. These experiments support field observations that, in some marine habitats, cuttlefish will respond to vertically oriented background features even when the preponderance of visual information in their field of view seems to be from the 2D surrounding substrate. Such choices highlight the selective decision-making that occurs in cephalopods with their adaptive camouflage capability.
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PreprintQuantification of cuttlefish (Sepia officinalis) camouflage : a study of color and luminance using in situ spectrometry( 2012-11-19)Cephalopods are renowned for their ability to adaptively camouflage on diverse backgrounds. Sepia officinalis camouflage body patterns have been characterized spectrally in the laboratory but not in the field due to the challenges of dynamic natural light fields and the difficulty of using spectrophotometric instruments underwater. To assess cuttlefish color match in their natural habitats, we studied the spectral properties of S. officinalis and their backgrounds on the Aegean coast of Turkey using point-by-point in situ spectrometry. Fifteen spectrometry datasets were collected from seven cuttlefish; radiance spectra from animal body components and surrounding substrates were measured at depths shallower than 5m. We quantified luminance and color contrast of cuttlefish components and background substrates in the eyes of hypothetical di- and trichromatic fish predators. Additionally, we converted radiance spectra to sRGB color space to simulate their in situ appearance to a human observer. Within the range of natural colors at our study site, cuttlefish closely matched the substrate spectra in a variety of body patterns. Theoretical calculations showed that this effect might be more pronounced at greater depths. We also showed that a non-biological method (“Spectral Angle Mapper”), commonly used for spectral shape similarity assessment in the field of remote sensing, shows moderate correlation to biological measures of color contrast. This performance is comparable to that of a traditional measure of spectral shape similarity, hue and chroma. This study is among the first to quantify color matching of camouflaged cuttlefish in the wild.