Bodily injury in mammals often produces persistent pain that is driven at least in part by long-l... more 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.
Survivable injuries are a common yet costly experience. The ability to sense and respond to noxio... more Survivable injuries are a common yet costly experience. The ability to sense and respond to noxious stimuli is an almost universal trait, and prolonged behavioral alterations, including sensitization to touch and other stimuli, may function to ameliorate fitness costs associated with injury. Cephalopods can modify their behavior by learned association with noxious electric shock, but nonassociative alterations of behavioral responses after tissue injury have not been studied. The aim of this study was to make the first systematic investigations in any cephalopod of behavioral responses and alterations elicited by explicit, minor injury. By testing responsiveness in the longfin squid, Loligo pealeii, to the approach and contact of an innocuous filament applied to different parts of the body both before and after injury to the distal third of one arm, we show that a cephalopod expresses behavioral alterations persisting for at least 2 days after injury. These alterations parallel forms of nociceptive plasticity in other animals, including general and site-specific sensitization to tactile stimuli. A novel finding is that hyper-responsiveness after injury extends to visual stimuli. Injured squid are more likely to employ crypsis than escape in response to an approaching visual stimulus shortly after injury, but initiate escape earlier and continue escape behaviors for longer when tested from 1 to 48h after injury. Injury failed to elicit overt wound-directed behavior (e.g. grooming) or change hunting success. Our results show that longlasting nociceptive sensitization occurs in cephalopods, and suggest that it may function to reduce predation risk after injury.
Cuttlefish are an important global fisheries resource, and their demand is placing increasing pre... more Cuttlefish are an important global fisheries resource, and their demand is placing increasing pressure on populations in many areas, necessitating conservation measures. We reviewed evidence from case studies spanning Europe, Africa, Asia, and Australia encompassing diverse intervention methods (fisheries closures, protected areas, habitat restoration, fishing-gear modifications, promoting egg survival, and restocking), and we also discuss the effects of pollution on cuttlefish. We conclude: (1) spatio-temporal closures need to encompass substantial portions of a species'
The visibility of cephalopod chromatophore organs is regulated dynamically by rosettes of oblique... more The visibility of cephalopod chromatophore organs is regulated dynamically by rosettes of obliquely striated radial muscles that dilate or relax the diameter of a central pigmented sacculus in 100–300 ms. Each of the several dozen muscles has a flared proximal end that adheres tightly to its pigmented sacculus and an extremely elongated distal end which branches into single fibrils that anchor into the dermis. This geometry provides ample opportunity for overlap of the many muscles from neighboring chromatophores. The temporal activity of these muscles has been believed to be patterned exclusively by monosynaptic projections from sets of efferent motor axons originating in the chromatophore lobes of the suboesophageal brain. Based on historical observations that distal radial muscles from some chromatophores appear to extend closely to muscles from other chromatophores, we asked whether radial muscles actually make specialized contacts. Using 3D electron microscopy of Doryteuthis pe...
This study investigated how cuttlefish (Sepia officinalis) camouflage patterns are influenced by ... more This study investigated how cuttlefish (Sepia officinalis) camouflage patterns are influenced by the proportions of different gray-scales present in visually cluttered environments. All experimental substrates comprised spatially random arrays of texture elements (texels) of five gray-scales: Black, Dark gray, Gray, Light gray, and White. The substrates in Experiment 1 were densely packed arrays of square texels that varied over 4 sizes in different conditions. Experiment 2 used substrates in which texels were disks separated on a homogeneous background that was Black, Gray or White in different conditions. In a given condition, the histogram of texel gray-scales was varied across different substrates. For each of 16 cuttlefish pattern response statistics c, the resulting data were used to determine the strength with which variations in the proportions of different gray-scales influenced c. The main finding is that darker-than-average texels (i.e., texels of negative contrast polarity) predominate in controlling cuttlefish pattern responses in the context of cluttered substrates. In Experiment 1, for example, substrates of all four texel-sizes, activation of the cuttlefish "white square" and "white head bar" (two highly salient skin components) is strongly influenced by variations in the proportions of Black and Dark gray (but not Gray, Light gray, or White) texels. It is hypothesized that in the context of high-variance visual input characteristic of cluttered substrates in the cuttlefish natural habitat, elements of negative contrast polarity reliably signal the presence of edges produced by overlapping objects, in the presence of which disruptive pattern responses are likely to achieve effective camouflage.
Chromatophore organs in cephalopod skin are known to produce ultra-fast changes in appearance for... more Chromatophore organs in cephalopod skin are known to produce ultra-fast changes in appearance for camouflage and communication. Light-scattering pigment granules within chromatocytes have been presumed to be the sole source of coloration in these complex organs. We report the discovery of structural coloration emanating in precise register with expanded pigmented chromatocytes. Concurrently, using an annotated squid chromatophore proteome together with microscopy, we identify a likely biochemical component of this reflective coloration as reflectin proteins distributed in sheath cells that envelop each chromatocyte. Additionally, within the chromatocytes, where the pigment resides in nanostructured granules, we find the lens protein Ω- crystallin interfacing tightly with pigment molecules. These findings offer fresh perspectives on the intricate biophotonic interplay between pigmentary and structural coloration elements tightly co-located within the same dynamic flexible organ - a f...
The highly diverse and changeable body patterns of cephalopods require the production of whitenes... more The highly diverse and changeable body patterns of cephalopods require the production of whiteness of varying degrees of brightness for their large repertoire of communication and camouflage behaviors. Leucophores are structural reflectors that produce whiteness in cephalopods; they are dermal aggregates of numerous leucocytes containing spherical leucosomes ranging in diameter from 200-2000 nm. In Sepia officinalis leucophores, leucocytes always occur in various combinations with iridocytes, cells containing plates that function as Bragg stacks to reflect light of particular wavelengths. Both spheres and plates contain the high-refractive-index protein reflectin. Four leucophore skin-patterning components were investigated morphologically and with spectrometry. In descending order of brightness they are: white fin spots, White zebra bands, White square, and White head bar. Different densities, thicknesses and proportions of leucocytes and iridocytes were correlated with the relativ...
Many animals produce multiple displays during agonistic interactions, but the roles of these disp... more Many animals produce multiple displays during agonistic interactions, but the roles of these displays often remain ambiguous. The hierarchical signaling hypothesis has been proposed to explain their occurrence and posits that different displays convey different levels of aggressive intent, allowing signalers to communicate graded series of threats. This hypothesis suggests that low-risk signals, typically performed at the beginning stages of an interaction, are strong predictors of high-risk signals but weak predictors of physical aggression. High-risk signals, typically produced at later stages of an interaction, are strong predictors of physical aggression. We used giant Australian cuttlefish, Sepia apama, to test these predictions. We combined field observations and laboratory video playback experiments to determine whether (i) male cuttlefish produce specific sequences of displays, (ii) displays in early stages of an interaction predict displays in later stages of an interaction, and (iii) displays produced in later stages of an interaction provide reliable predictors of physical aggression. Field observations suggested that males progressed from low-risk to high-risk signals (i.e., visual signaling to physical aggression). Video playback results zrevealed that the low-risk frontal display, produced during early stages of an interaction, conveys reliable information about the cuttlefish’s intent to escalate to later stages of visual signaling. Both the shovel and lateral displays were produced during the later stages of signaling and were reliable predictors of subsequent physical aggression. Our study supports the hierarchical signaling hypothesis and provides new empirical insights into how cuttlefish use progressive visual signaling to convey increasing levels of threat.Significance statementMany animals perform multiple displays during fights, but the roles of these displays often remain ambiguous. The hierarchical signaling hypothesis posits that animals produce multiple displays to convey different levels of aggressive intent, allowing signalers to communicate graded series of threats. We tested this hypothesis in giant Australian cuttlefish, Sepia apama. Specifically, we tested whether (i) displays in early stages of a fight predict displays in later stages of a fight and (ii) displays produced in later stages of a fight provide reliable predictors of physical aggression. Our results support these predictions and reveal that fighting cuttlefish progress from low-risk signals to high-risk signals to convey a hierarchy of threats. This study highlights the generality of hierarchical signaling during animal contests, as cuttlefish are evolutionary far removed from many of the species that have been reported to use this type of signaling.
2009 IEEE International Conference on Robotics and Automation, 2009
This paper describes a recent study in which an Autonomous Underwater Vehicle (AUV) with a high r... more This paper describes a recent study in which an Autonomous Underwater Vehicle (AUV) with a high resolution stereo-imaging system was used to document nocturnal camouflage behaviour in cuttlefish at a well known spawning site in Whyalla, South Australia. The AUV's ability to fly at low altitude during day and night while closely following a desired survey pattern provided improved data collection compared to divers and previous work with a small ROV. Over the course of the week long expedition, the AUV Sirius was deployed on 38 dives at three sites in the survey area and collected tens of thousands of stereo images. Of these, nearly a thousand were seen to contain cuttlefish during post cruise analysis, with a large proportion showing evidence of camouflage. The distribution of images containing cuttlefish suggest that the animal concentrations were substantially higher closer in to shore in shallow waters, where the flat rocky substrate occurs; females lay their eggs on the underside of these rocks. Results demonstrate the strengths of using an AUV for surveying nearshore benthic habitats of ecological interest, with a particular emphasis on the ability to operate during both day and night time operations.
Animals attempt to maximize their reproductive fitness by employing discrimination tactics that i... more Animals attempt to maximize their reproductive fitness by employing discrimination tactics that increase their fertilization success. Semelparous species are faced with high energy and time constraints. These constraints are predicted to affect the extent of discrimination tactics that may be employed. The semelparous giant Australian cuttlefish, Sepia apama, seek multiple mates during their single breeding season, yet the discrimination tactics used to assess mates remain ambiguous. We combined field observations and laboratory-controlled mating experiments to determine (i) the relationship between the female signal (i.e., white lateral stripe) and mating outcome and (ii) the effects of the white lateral stripe, receptive postures, mating history, and familiarity on mating behavior. Females were less likely to mate when they expressed the white lateral stripe, suggesting that this signal conveys non-receptivity. Female mating history appeared to predict their likelihood of mating because females that had not recently mated were more likely to perform receptive postures and less likely to express the white lateral stripe. Familiarity with the males did not affect female expression of the white lateral stripe nor receptive postures. In males, mating behavior was not affected by the females' expression of the white lateral stripe nor female receptive postures; however, familiarity with the female did affect male mating behavior. Males exerted a strong preference for unfamiliar females, providing evidence for familiarity discrimination. This research suggests that distinct selection pressures may be driving different discrimination capabilities in the sexes and provides the first empirical evidence of familiarity discrimination in a cephalopod species.
9 Rapid adaptive camouflage in cephalopods 9.1 Roger T. Hanlon, Chuan-Chin C. Chiao, Lydia M. Mat... more 9 Rapid adaptive camouflage in cephalopods 9.1 Roger T. Hanlon, Chuan-Chin C. Chiao, Lydia M. Mathger, Kendra C. Buresch, Alexandra Barbosa, Justine J. Allen, Liese Siemann and Charles Chubb Camouflage versatility is probably no better ... 2005, 2007; Kelman et al. ...
Squid display impressive changes in body coloration that are afforded by two types of dynamic ski... more Squid 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: (1) the iridescence signals are routed through a peripheral center called the stellate ganglion and (2) the iridescence motor neurons 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 togeth...
Disruptive body coloration is a primary camouflage tactic of cuttlefish. Because rapid changeable... more Disruptive body coloration is a primary camouflage tactic of cuttlefish. Because rapid changeable coloration of cephalopods is guided visually, we can present different visual backgrounds (e.g., computer-generated, two-dimensional prints) and video record the animal's response by describing and grading its body pattern. We showed previously that strength of cuttlefish disruptive patterning depends on the size, contrast, and density of discrete
Coleoid cephalopods adaptively change their body patterns (color, contrast, locomotion, posture, ... more Coleoid cephalopods adaptively change their body patterns (color, contrast, locomotion, posture, and texture) for camouflage and signaling. Benthic octopuses and cuttlefish possess the capability, unique in the animal kingdom, to dramatically and quickly change their skin from smooth and flat to rugose and three‐dimensional. The organs responsible for this physical change are the skin papillae, whose biomechanics have not been investigated. In this study, small dorsal papillae from cuttlefish (Sepia officinalis) were preserved in their retracted or extended state, and examined with a variety of histological techniques including brightfield, confocal, and scanning electron microscopy. Analyses revealed that papillae are composed of an extensive network of dermal erector muscles, some of which are arranged in concentric rings while others extend across each papilla's diameter. Like cephalopod arms, tentacles, and suckers, skin papillae appear to function as muscular hydrostats. Th...
A major component of cephalopod adaptive camouflage behavior has rarely been studied: their abili... more A major component of cephalopod adaptive camouflage behavior has rarely been studied: their ability to change the three-dimensionality of their skin by morphing their malleable dermal papillae. Recent work has established that simple, conical papillae in cuttlefish (Sepia officinalis) function as muscular hydrostats; that is, the muscles that extend a papilla also provide its structural support. We used brightfield and scanning electron microscopy to investigate and compare the functional morphology of nine types of papillae of different shapes, sizes and complexity in six species: S. officinalis small dorsal papillae, Octopus vulgaris small dorsal and ventral eye papillae, Macrotritopus defilippi dorsal eye papillae, Abdopus aculeatus major mantle papillae, O. bimaculoides arm, minor mantle, and dorsal eye papillae, and S. apama face ridge papillae. Most papillae have two sets of muscles responsible for extension: circular dermal erector muscles arranged in a concentric pattern to lift the papilla away from the body surface and horizontal dermal erector muscles to pull the papilla's perimeter toward its core and determine shape. A third set of muscles, retractors, appears to be responsible for pulling a papilla's apex down toward the body surface while stretching out its base. Connective tissue infiltrated with mucopolysaccharides assists with structural support. S. apama face ridge papillae are different: the contraction of erector muscles perpendicular to the ridge causes overlying tissues to buckle. In this case, mucopolysaccharide-rich connective tissue provides structural support. These six species possess changeable papillae that are diverse in size and shape, yet with one exception they share somewhat similar functional morphologies. Future research on papilla morphology, biomechanics and neural control in the many unexamined species of octopus and cuttlefish may uncover new principles of actuation in soft, flexible tissue.
Bodily injury in mammals often produces persistent pain that is driven at least in part by long-l... more 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.
Survivable injuries are a common yet costly experience. The ability to sense and respond to noxio... more Survivable injuries are a common yet costly experience. The ability to sense and respond to noxious stimuli is an almost universal trait, and prolonged behavioral alterations, including sensitization to touch and other stimuli, may function to ameliorate fitness costs associated with injury. Cephalopods can modify their behavior by learned association with noxious electric shock, but nonassociative alterations of behavioral responses after tissue injury have not been studied. The aim of this study was to make the first systematic investigations in any cephalopod of behavioral responses and alterations elicited by explicit, minor injury. By testing responsiveness in the longfin squid, Loligo pealeii, to the approach and contact of an innocuous filament applied to different parts of the body both before and after injury to the distal third of one arm, we show that a cephalopod expresses behavioral alterations persisting for at least 2 days after injury. These alterations parallel forms of nociceptive plasticity in other animals, including general and site-specific sensitization to tactile stimuli. A novel finding is that hyper-responsiveness after injury extends to visual stimuli. Injured squid are more likely to employ crypsis than escape in response to an approaching visual stimulus shortly after injury, but initiate escape earlier and continue escape behaviors for longer when tested from 1 to 48h after injury. Injury failed to elicit overt wound-directed behavior (e.g. grooming) or change hunting success. Our results show that longlasting nociceptive sensitization occurs in cephalopods, and suggest that it may function to reduce predation risk after injury.
Cuttlefish are an important global fisheries resource, and their demand is placing increasing pre... more Cuttlefish are an important global fisheries resource, and their demand is placing increasing pressure on populations in many areas, necessitating conservation measures. We reviewed evidence from case studies spanning Europe, Africa, Asia, and Australia encompassing diverse intervention methods (fisheries closures, protected areas, habitat restoration, fishing-gear modifications, promoting egg survival, and restocking), and we also discuss the effects of pollution on cuttlefish. We conclude: (1) spatio-temporal closures need to encompass substantial portions of a species'
The visibility of cephalopod chromatophore organs is regulated dynamically by rosettes of oblique... more The visibility of cephalopod chromatophore organs is regulated dynamically by rosettes of obliquely striated radial muscles that dilate or relax the diameter of a central pigmented sacculus in 100–300 ms. Each of the several dozen muscles has a flared proximal end that adheres tightly to its pigmented sacculus and an extremely elongated distal end which branches into single fibrils that anchor into the dermis. This geometry provides ample opportunity for overlap of the many muscles from neighboring chromatophores. The temporal activity of these muscles has been believed to be patterned exclusively by monosynaptic projections from sets of efferent motor axons originating in the chromatophore lobes of the suboesophageal brain. Based on historical observations that distal radial muscles from some chromatophores appear to extend closely to muscles from other chromatophores, we asked whether radial muscles actually make specialized contacts. Using 3D electron microscopy of Doryteuthis pe...
This study investigated how cuttlefish (Sepia officinalis) camouflage patterns are influenced by ... more This study investigated how cuttlefish (Sepia officinalis) camouflage patterns are influenced by the proportions of different gray-scales present in visually cluttered environments. All experimental substrates comprised spatially random arrays of texture elements (texels) of five gray-scales: Black, Dark gray, Gray, Light gray, and White. The substrates in Experiment 1 were densely packed arrays of square texels that varied over 4 sizes in different conditions. Experiment 2 used substrates in which texels were disks separated on a homogeneous background that was Black, Gray or White in different conditions. In a given condition, the histogram of texel gray-scales was varied across different substrates. For each of 16 cuttlefish pattern response statistics c, the resulting data were used to determine the strength with which variations in the proportions of different gray-scales influenced c. The main finding is that darker-than-average texels (i.e., texels of negative contrast polarity) predominate in controlling cuttlefish pattern responses in the context of cluttered substrates. In Experiment 1, for example, substrates of all four texel-sizes, activation of the cuttlefish "white square" and "white head bar" (two highly salient skin components) is strongly influenced by variations in the proportions of Black and Dark gray (but not Gray, Light gray, or White) texels. It is hypothesized that in the context of high-variance visual input characteristic of cluttered substrates in the cuttlefish natural habitat, elements of negative contrast polarity reliably signal the presence of edges produced by overlapping objects, in the presence of which disruptive pattern responses are likely to achieve effective camouflage.
Chromatophore organs in cephalopod skin are known to produce ultra-fast changes in appearance for... more Chromatophore organs in cephalopod skin are known to produce ultra-fast changes in appearance for camouflage and communication. Light-scattering pigment granules within chromatocytes have been presumed to be the sole source of coloration in these complex organs. We report the discovery of structural coloration emanating in precise register with expanded pigmented chromatocytes. Concurrently, using an annotated squid chromatophore proteome together with microscopy, we identify a likely biochemical component of this reflective coloration as reflectin proteins distributed in sheath cells that envelop each chromatocyte. Additionally, within the chromatocytes, where the pigment resides in nanostructured granules, we find the lens protein Ω- crystallin interfacing tightly with pigment molecules. These findings offer fresh perspectives on the intricate biophotonic interplay between pigmentary and structural coloration elements tightly co-located within the same dynamic flexible organ - a f...
The highly diverse and changeable body patterns of cephalopods require the production of whitenes... more The highly diverse and changeable body patterns of cephalopods require the production of whiteness of varying degrees of brightness for their large repertoire of communication and camouflage behaviors. Leucophores are structural reflectors that produce whiteness in cephalopods; they are dermal aggregates of numerous leucocytes containing spherical leucosomes ranging in diameter from 200-2000 nm. In Sepia officinalis leucophores, leucocytes always occur in various combinations with iridocytes, cells containing plates that function as Bragg stacks to reflect light of particular wavelengths. Both spheres and plates contain the high-refractive-index protein reflectin. Four leucophore skin-patterning components were investigated morphologically and with spectrometry. In descending order of brightness they are: white fin spots, White zebra bands, White square, and White head bar. Different densities, thicknesses and proportions of leucocytes and iridocytes were correlated with the relativ...
Many animals produce multiple displays during agonistic interactions, but the roles of these disp... more Many animals produce multiple displays during agonistic interactions, but the roles of these displays often remain ambiguous. The hierarchical signaling hypothesis has been proposed to explain their occurrence and posits that different displays convey different levels of aggressive intent, allowing signalers to communicate graded series of threats. This hypothesis suggests that low-risk signals, typically performed at the beginning stages of an interaction, are strong predictors of high-risk signals but weak predictors of physical aggression. High-risk signals, typically produced at later stages of an interaction, are strong predictors of physical aggression. We used giant Australian cuttlefish, Sepia apama, to test these predictions. We combined field observations and laboratory video playback experiments to determine whether (i) male cuttlefish produce specific sequences of displays, (ii) displays in early stages of an interaction predict displays in later stages of an interaction, and (iii) displays produced in later stages of an interaction provide reliable predictors of physical aggression. Field observations suggested that males progressed from low-risk to high-risk signals (i.e., visual signaling to physical aggression). Video playback results zrevealed that the low-risk frontal display, produced during early stages of an interaction, conveys reliable information about the cuttlefish’s intent to escalate to later stages of visual signaling. Both the shovel and lateral displays were produced during the later stages of signaling and were reliable predictors of subsequent physical aggression. Our study supports the hierarchical signaling hypothesis and provides new empirical insights into how cuttlefish use progressive visual signaling to convey increasing levels of threat.Significance statementMany animals perform multiple displays during fights, but the roles of these displays often remain ambiguous. The hierarchical signaling hypothesis posits that animals produce multiple displays to convey different levels of aggressive intent, allowing signalers to communicate graded series of threats. We tested this hypothesis in giant Australian cuttlefish, Sepia apama. Specifically, we tested whether (i) displays in early stages of a fight predict displays in later stages of a fight and (ii) displays produced in later stages of a fight provide reliable predictors of physical aggression. Our results support these predictions and reveal that fighting cuttlefish progress from low-risk signals to high-risk signals to convey a hierarchy of threats. This study highlights the generality of hierarchical signaling during animal contests, as cuttlefish are evolutionary far removed from many of the species that have been reported to use this type of signaling.
2009 IEEE International Conference on Robotics and Automation, 2009
This paper describes a recent study in which an Autonomous Underwater Vehicle (AUV) with a high r... more This paper describes a recent study in which an Autonomous Underwater Vehicle (AUV) with a high resolution stereo-imaging system was used to document nocturnal camouflage behaviour in cuttlefish at a well known spawning site in Whyalla, South Australia. The AUV's ability to fly at low altitude during day and night while closely following a desired survey pattern provided improved data collection compared to divers and previous work with a small ROV. Over the course of the week long expedition, the AUV Sirius was deployed on 38 dives at three sites in the survey area and collected tens of thousands of stereo images. Of these, nearly a thousand were seen to contain cuttlefish during post cruise analysis, with a large proportion showing evidence of camouflage. The distribution of images containing cuttlefish suggest that the animal concentrations were substantially higher closer in to shore in shallow waters, where the flat rocky substrate occurs; females lay their eggs on the underside of these rocks. Results demonstrate the strengths of using an AUV for surveying nearshore benthic habitats of ecological interest, with a particular emphasis on the ability to operate during both day and night time operations.
Animals attempt to maximize their reproductive fitness by employing discrimination tactics that i... more Animals attempt to maximize their reproductive fitness by employing discrimination tactics that increase their fertilization success. Semelparous species are faced with high energy and time constraints. These constraints are predicted to affect the extent of discrimination tactics that may be employed. The semelparous giant Australian cuttlefish, Sepia apama, seek multiple mates during their single breeding season, yet the discrimination tactics used to assess mates remain ambiguous. We combined field observations and laboratory-controlled mating experiments to determine (i) the relationship between the female signal (i.e., white lateral stripe) and mating outcome and (ii) the effects of the white lateral stripe, receptive postures, mating history, and familiarity on mating behavior. Females were less likely to mate when they expressed the white lateral stripe, suggesting that this signal conveys non-receptivity. Female mating history appeared to predict their likelihood of mating because females that had not recently mated were more likely to perform receptive postures and less likely to express the white lateral stripe. Familiarity with the males did not affect female expression of the white lateral stripe nor receptive postures. In males, mating behavior was not affected by the females' expression of the white lateral stripe nor female receptive postures; however, familiarity with the female did affect male mating behavior. Males exerted a strong preference for unfamiliar females, providing evidence for familiarity discrimination. This research suggests that distinct selection pressures may be driving different discrimination capabilities in the sexes and provides the first empirical evidence of familiarity discrimination in a cephalopod species.
9 Rapid adaptive camouflage in cephalopods 9.1 Roger T. Hanlon, Chuan-Chin C. Chiao, Lydia M. Mat... more 9 Rapid adaptive camouflage in cephalopods 9.1 Roger T. Hanlon, Chuan-Chin C. Chiao, Lydia M. Mathger, Kendra C. Buresch, Alexandra Barbosa, Justine J. Allen, Liese Siemann and Charles Chubb Camouflage versatility is probably no better ... 2005, 2007; Kelman et al. ...
Squid display impressive changes in body coloration that are afforded by two types of dynamic ski... more Squid 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: (1) the iridescence signals are routed through a peripheral center called the stellate ganglion and (2) the iridescence motor neurons 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 togeth...
Disruptive body coloration is a primary camouflage tactic of cuttlefish. Because rapid changeable... more Disruptive body coloration is a primary camouflage tactic of cuttlefish. Because rapid changeable coloration of cephalopods is guided visually, we can present different visual backgrounds (e.g., computer-generated, two-dimensional prints) and video record the animal's response by describing and grading its body pattern. We showed previously that strength of cuttlefish disruptive patterning depends on the size, contrast, and density of discrete
Coleoid cephalopods adaptively change their body patterns (color, contrast, locomotion, posture, ... more Coleoid cephalopods adaptively change their body patterns (color, contrast, locomotion, posture, and texture) for camouflage and signaling. Benthic octopuses and cuttlefish possess the capability, unique in the animal kingdom, to dramatically and quickly change their skin from smooth and flat to rugose and three‐dimensional. The organs responsible for this physical change are the skin papillae, whose biomechanics have not been investigated. In this study, small dorsal papillae from cuttlefish (Sepia officinalis) were preserved in their retracted or extended state, and examined with a variety of histological techniques including brightfield, confocal, and scanning electron microscopy. Analyses revealed that papillae are composed of an extensive network of dermal erector muscles, some of which are arranged in concentric rings while others extend across each papilla's diameter. Like cephalopod arms, tentacles, and suckers, skin papillae appear to function as muscular hydrostats. Th...
A major component of cephalopod adaptive camouflage behavior has rarely been studied: their abili... more A major component of cephalopod adaptive camouflage behavior has rarely been studied: their ability to change the three-dimensionality of their skin by morphing their malleable dermal papillae. Recent work has established that simple, conical papillae in cuttlefish (Sepia officinalis) function as muscular hydrostats; that is, the muscles that extend a papilla also provide its structural support. We used brightfield and scanning electron microscopy to investigate and compare the functional morphology of nine types of papillae of different shapes, sizes and complexity in six species: S. officinalis small dorsal papillae, Octopus vulgaris small dorsal and ventral eye papillae, Macrotritopus defilippi dorsal eye papillae, Abdopus aculeatus major mantle papillae, O. bimaculoides arm, minor mantle, and dorsal eye papillae, and S. apama face ridge papillae. Most papillae have two sets of muscles responsible for extension: circular dermal erector muscles arranged in a concentric pattern to lift the papilla away from the body surface and horizontal dermal erector muscles to pull the papilla's perimeter toward its core and determine shape. A third set of muscles, retractors, appears to be responsible for pulling a papilla's apex down toward the body surface while stretching out its base. Connective tissue infiltrated with mucopolysaccharides assists with structural support. S. apama face ridge papillae are different: the contraction of erector muscles perpendicular to the ridge causes overlying tissues to buckle. In this case, mucopolysaccharide-rich connective tissue provides structural support. These six species possess changeable papillae that are diverse in size and shape, yet with one exception they share somewhat similar functional morphologies. Future research on papilla morphology, biomechanics and neural control in the many unexamined species of octopus and cuttlefish may uncover new principles of actuation in soft, flexible tissue.
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Papers by Roger Hanlon