Dan-Eric Nilsson

Box Jellyfish Use Terrestrial Visual Cues for Navigation

Box jellyfish have an impressive set of 24 eyes of four different types, including eyes structurally similar to those of vertebrates and cephalopods [1, 2]. However, the known visual responses are restricted to simple phototaxis, shadow responses, and object avoidance responses [3-8], and it has been a puzzle why they need such a complex set of eyes. Here we report that medusae of the box jellyfish Tripedalia cystophora are capable of visually guided navigation in mangrove swamps using terrestrial structures seen through the water surface. They detect the mangrove canopy by an eye type that is specialized to peer up through the water surface and that is suspended such that it is constantly looking straight up, irrespective of the orientation of the jellyfish. The visual information is used to navigate to the preferred habitat at the edge of mangrove lagoons.

A Unique Advantage for Giant Eyes in Giant Squid.

Giant and colossal deep-sea squid (Architeuthis and Mesonychoteuthis) have the largest eyes in the animal kingdom [1, 2], but there is no explanation for why they would need eyes that are nearly three times the diameter of those of any other extant animal. Here we develop a theory for visual detection in pelagic habitats, which predicts that such giant eyes are unlikely to evolve for detecting mates or prey at long distance but are instead uniquely suited for detecting very large predators, such as sperm whales. We also provide photographic documentation of an eyeball of about 27 cm with a 9 cm pupil in a giant squid, and we predict that, below 600 m depth, it would allow detection of sperm whales at distances exceeding 120 m. With this long range of vision, giant squid get an early warning of approaching sperm whales. Because the sonar range of sperm whales exceeds 120 m [3-5], we hypothesize that a well-prepared and powerful evasive response to hunting sperm whales may have driven the evolution of huge dimensions in both eyes and bodies of giant and colossal squid. Our theory also provides insights into the vision of Mesozoic ichthyosaurs with unusually large eyes.

Superior Underwater Vision in a Human Population of Sea Gypsies

Humans are poorly adapted for underwater vision. In air, the curved corneal surface accounts for two-thirds of the eyes refractive power, and this is lost when air is replaced by water. Despite this, some tribes of sea gypsies in Southeast Asia live off the sea, and the children collect food from the sea floor without the use of visual aids. This is a remarkable feat when one considers that the human eye is not focused underwater and small objects should remain unresolved. We have measured the visual acuity of children in a sea gypsy population, the Moken, and found that the children see much better underwater than one might expect. Their underwater acuity (6.06 cycles/degree) is more than twice as good as that of European children (2.95 cycles/degree). Our investigations show that the Moken children achieve their superior underwater vision by maximally constricting the pupil (1.96 mm compared to 2.50 mm in European children) and by accommodating to the known limit of human performance (15-16 D). This extreme reaction-which is routine in Moken children-is completely absent in European children. Because they are completely dependent on the sea, the Moken are very likely to derive great benefit from this strategy.

The spectral sensitivity of the lens eyes of a box jellyfish, Tripedalia cystophora (Conant)

SUMMARY Box jellyfish, or cubomedusae (class Cubozoa), are unique among the Cnidaria in possessing lens eyes similar in morphology to those of vertebrates and cephalopods. Although these eyes were described over 100 years ago, there has been no work done on their electrophysiological responses to light. We used an electroretinogram (ERG) technique to measure spectral sensitivity of the lens eyes of the Caribbean species Tripedalia cystophora. The cubomedusae have two kinds of lens eyes, the lower and upper lens eyes. We found that both lens eye types have similar spectral sensitivities, which likely result from the presence of a single receptor type containing a single opsin. The peak sensitivity is to blue-green light. Visual pigment template fits indicate a vitamin A-1 based opsin with peak sensitivity near 500 nm for both eye types.

Visual navigation in starfish: first evidence for the use of vision and eyes in starfish

Most known starfish species possess a compound eye at the tip of each arm, which, except for the lack of true optics, resembles an arthropod compound eye. Although these compound eyes have been known for about two centuries, no visually guided behaviour has ever been directly associated with their presence. There are indications that they are involved in negative phototaxis but this may also be governed by extraocular photoreceptors. Here, we show that the eyes of the coral-reef-associated starfish Linckia laevigata are slow and colour blind. The eyes are capable of true image formation although with low spatial resolution. Further, our behavioural experiments reveal that only specimens with intact eyes can navigate back to their reef habitat when displaced, demonstrating that this is a visually guided behaviour. This is, to our knowledge, the first report of a function of starfish compound eyes. We also show that the spectral sensitivity optimizes the contrast between the reef and the open ocean. Our results provide an example of an eye supporting only low-resolution vision, which is believed to be an essential stage in eye evolution, preceding the high-resolution vision required for detecting prey, predators and conspecifics.

Bilateral symmetric organization of neural elements in the visual system of a coelenterate, Tripedalia cystophora (Cubozoa)

Cubozoans differ from other cnidarians by their body architecture and nervous system structure. In the medusa stage they possess the most advanced visual system within the phylum, located in sophisticated sensory structures, rhopalia. The rhopalium is a club‐shaped structure with paired pit‐shaped pigment cup eyes, paired slit‐shaped pigment cup eyes, and two complex camera‐type eyes: one small upper lens eye and one large lower lens eye. The medusa carries four rhopalia and visual processing and locomotor rhythm generation takes place in the rhopalia. We show here a bilaterally symmetric organization of neurons, with commissures connecting the two sides, in the rhopalium of the cubozoan Tripedalia cystophora. The fortuitous observation that a subset of neurons is strongly immunoreactive for a PCNA (proliferating cell nuclear antigen)‐like epitope allowed us to analyze the organization of these neurons in detail. Distinct PCNA‐immunoreactive (PCNA‐ir) nuclei form six bilateral pairs that are associated with the slit eyes, pit eyes, upper lens eye, and the posterior wall of the rhopalium. Three commissures connect the clusters of the two sides and all clusters in the rhopalium have connections to the area around the base of the stalk. This neuronal system provides an anatomical substrate for integration of visual signals from the different eyes. J. Comp. Neurol. 492:251–262, 2005.

A new mechanism for light-dark adaptation in theArtemia compound eye (Anostraca, Crustacea)

SummaryThe apposition compound eye ofArtemia sp. (a brine shrimp) has a glycogen lens inside the crystalline cone. Owing to the absence of a corneal lens, the glycogen lens is solely responsible for the focusing on the rhabdom tip. Examination of the light-dark adaptation mechanism revealed the following:1.No pigment migration and only small changes in the palisade.2.A slight increase in diameter of the distal part of the rhabdom during dark adaptation.3.A pronounced shortening of the cone during dark adaptation, resulting in a reduced distance between the glycogen lens and the rhabdom.4.Simultaneous with (3), the glycogen lens elongates as the radii of curvature of the refracting surfaces decrease. A careful optical investigation of the adaptational mechanism demonstrated perfectly focused ommatidia irrespective of the adaptational length of the cone. The refocusing is performed by the curvature change of the glycogen lens. This results in a change in focal length of the system, and thus an adjustable acceptance angle. The change in rhabdom diameter increases the change in the acceptance angle.The optics of ommatidia in different parts of the eye was analysed in order to evaluate the extent of regional differences.A method for refractive index measurements in living cells, including viability tests, is described, and the importance of suitable immersion media is discussed.

Visual control of steering in the box jellyfish Tripedalia cystophora

SUMMARY Box jellyfish carry an elaborate visual system consisting of 24 eyes, which they use for driving a number of behaviours. However, it is not known how visual input controls the swimming behaviour. In this study we exposed the Caribbean box jellyfish Tripedalia cystophora to simple visual stimuli and recorded changes in their swimming behaviour. Animals were tethered in a small experimental chamber, where we could control lighting conditions. The behaviour of the animals was quantified by tracking the movements of the bell, using a high-speed camera. We found that the animals respond predictably to the darkening of one quadrant of the equatorial visual world by (1) increasing pulse frequency, (2) creating an asymmetry in the structure that constricts the outflow opening of the bell, the velarium, and (3) delaying contraction at one of the four sides of the bell. This causes the animals to orient their bell in such a way that, if not tethered, they would turn and swim away from the dark area. We conclude that the visual system of T. cystophora has a predictable effect on swimming behaviour.

The compound eye of Leptodora kindtii (Cladocera). An adaptation to planktonic life.

SummaryEach of the approximately 500 ommatidia in the compound eye of the cladoceran crustacean Leptodora kindtii has a crystalline cone consisting of five cells. Five retinula cells are also present, one of which contributes to the distal 1–2 μm of the rhabdom only; the other four retinula cells form a continuous rhabdom. Throughout the rhabdom its cross section displays two separate halves with the axis of the microvilli in one half perpendicular to that in the other (orthogonal pattern). Interferometric analysis of the refractive index of the crystalline cone revealed an inhomogeneous system with one distal and one proximal gradient. The gradient system was found to exclude rays entering from adjacent facets, thus maintaining the optical isolation. Consequently, these optics replace distal screening pigment, which is absent in the eye. The long and unscreened crystalline cones give rise to an almost transparent eye in conformity with the overall transparency of this planktonic animal.The morphological characteristics of the eye of this species deviate from other cladoceran eyes, but the optical design closely resembles that of some pelagic marine amphipod crustaceans.

Iso-luminance counterillumination drove bioluminescent shark radiation

Counterilluminating animals use ventral photogenic organs (photophores) to mimic the residual downwelling light and cloak their silhouette from upward-looking predators. To cope with variable conditions of pelagic light environments they typically adjust their luminescence intensity. Here, we found evidence that bioluminescent sharks instead emit a constant light output and move up and down in the water column to remain cryptic at iso-luminance depth. We observed, across 21 globally distributed shark species, a correlation between capture depth and the proportion of a ventral area occupied by photophores. This information further allowed us, using visual modelling, to provide an adaptive explanation for shark photophore pattern diversity: in species facing moderate predation risk from below, counterilluminating photophores were partially co-opted for bioluminescent signalling, leading to complex patterns. In addition to increase our understanding of pelagic ecosystems our study emphasizes the importance of bioluminescence as a speciation driver.