Günther Fleissner

Ultrastructural analysis of a putative magnetoreceptor in the beak of homing pigeons

With the use of different light and electron microscopic methods, we investigated the subcellular organization of afferent trigeminal terminals in the upper beak of the homing pigeon, Columba livia, which are about 5 μm in diameter and contain superparamagnetic magnetite (SPM) crystals. The SPM nanocrystals are assembled in clusters (diameter, ∼1–2 μm). About 10 to 15 of these clusters occur inside one nerve terminal, arranged along the cell membrane. Each SPM cluster is embedded in a solid fibrous cup, open towards the cell surface, to which the cluster adheres by delicate fiber strands. In addition to the SPM clusters, a second inorganic iron compound has been identified: noncrystalline platelets of iron phosphate (about 500 nm wide and long and maximally 100 nm thick) that occur along a fibrous core of the terminal. The anatomic features suggested that these nerve endings could detect small intensity changes of the geomagnetic field. Such stimuli can induce deformations of the SPM clusters, which could be transduced into primary receptor potentials by mechanosensitive membrane receptor channels. The subepidermal fat cells surrounding the nerve endings prevent the inside from external mechanical stimuli. These structural findings corresponded to conclusions inferred from rock magnetic measurements, theoretical calculations, model experiments, and behavioral data, which also matched previous electrophysiologic recordings from migratory birds. J. Comp. Neurol. 458:350–360, 2003.

A novel concept of Fe-mineral-based magnetoreception: histological and physicochemical data from the upper beak of homing pigeons

Animals make use of the Earth’s magnetic field for navigation and regulation of vegetative functions; however, the anatomical and physiological basis for the magnetic sense has not been elucidated yet. Our recent results from histology and X-ray analyses support the hypothesis that delicate iron-containing structures in the skin of the upper beak of homing pigeons might serve as a biological magnetometer. Histology has revealed various iron sites within dendrites of the trigeminal nerve, their arrangement along strands of axons, the existence of three dendritic fields in each side of the beak with specific 3D-orientations, and the bilateral symmetry of the whole system. Element mapping by micro-synchrotron X-ray fluorescence analysis has shown the distribution of iron and its quantities. Micro-synchrotron X-ray absorption near-edge-structure spectroscopy has allowed us to unambiguously identify maghemite as the predominating iron mineral (90 vs 10% magnetite). In this paper, we show that iron-based magnetoreception needs the presence of both of these iron minerals, their specific dimensions, shapes, and arrangements in three different subcellular compartments. We suggest that an inherent magnetic enhancement process via an iron-crusted vesicle and the attached chains of iron platelets might be sufficient to account for the sensitivity and specificity required by such a magnetoreceptor. The appropriate alignment between the Earth’s magnetic field and the maghemite bands would induce a multiple attraction of the magnetite bullets perpendicular to the membrane, thus, triggering strain-sensitive membrane channels and a primary receptor potential. Due to its 3D architecture and physicochemical nature, the dendritic system should be able to separately sense the three vector components of the Earth’s local field, simultaneously—allowing birds to detect their geographic position by the magnetic vector, i.e., amplitude and direction of the local magnetic field, irrespective of the animal’s posture or movement and photoreception.

A new model for a magnetoreceptor in homing pigeons based on interacting clusters of superparamagnetic magnetite

We present a new model of magnetic-field reception in magnetite-containing nerve terminals, which have recently been identified in the upper-beak skin of homing pigeons. The potentially magnetoreceptive nerve cells comprise chain-like aggregates with up to 20 closely spaced clusters of superparamagnetic (SP) magnetite. We designed experiments on superparamagnetic model systems to simulate the behaviour of the aggregates in varying magnetic fields. Magnetic-field induced interactions between the clusters in an aggregate gives rise to attractive and repulsive forces between the clusters. The resulting stress on the surrounding cellular structures varies with field direction and intensity. Our model is able to explain the principal features of the magnetic sense in homing pigeons as derived from behavioural experiments.

The optic nerve mediates the circadian pigment migration in the median eyes of the scorpion

Abstract 1. 1. The peripheral visual pathway from the median eyes of the scorpion Androctonus australis was interrupted at different points and the effect on the circadian rhythm of median-eye sensitivity was examined. 2. 2. Any interruption of the visual pathway distal to the supraesophageal ganglion abolishes the circadian sensitivity rhythm in the median eyes. This rhythm is thus controlled by efferents in the optic nerve (very probably via the neurosecretory axons) rather than by way of the hemolymph. 3. 3. Following transection of the optic nerve, the sensitivity of the median eyes proceeds rapidly to the daytime state. This condition is associated with movement of the screening pigment into the distal ends of the visual cells. 4. 4. The oscillator system controlling the circadian pigment migration in the median eye cannot be located in the eye itself, but must lie in the CNS, proximal to the first optic ganglion. The oscillator itself need not be connected to both median eyes in order to function normally, as revealed by the continued rhythm in the contralateral eye following unilateral optic nerve section.

A new type of putative non-visual photoreceptors in the optic lobe of beetles

A putative photoreceptor organ is described in the carabid beetle, Pachymorpha sexguttata. The elongated structure, about 20–40 μm wide and more than 300 μm long, is situated within the optic lobe at the fronto-dorsal rim of the lamina. It lies, deep in the head capsule, in front of the compound eyes and beneath window-like thinnings of the cuticle. The organ is composed of two types of cells: (1) clear sheath cells and (2) well-organized inner receptor cells that appear in a horseshoe-like or circular array in cross-section. Common histological features of all inner cells include a distal trunk ending in microvilli that form a rhabdom-like structure, an axon at the proximal end of the cell, lamellar and multivesicular bodies within the trunk, and clusters of small mitochondria. The organ has no shielding pigment. It is connected by thin axons to a circumscribed neuropil that parallels the organ, and thence via a fiber tract to the medulla accessoria, a possible site of the circadian pacemaker in insects. Immunoreactivity to anti-pers, an antibody recognizing the Drosophila period (per) protein that plays a central role in the function of the circadian pacemaker in fruit flies, is demonstratable in thin efferent terminals within the organ, in the associated neuropil and in its fiber connection to the medulla. A second receptor organ displaying the same fine structure lies near the second optic chiasm. This set of putative photoreceptors also occurs in the tenebrionid beetle, Zophobas morio, and its pupa. The possible function of these receptor organs is discussed with respect to former chronobiological data and some recently described types of extraretinal photoreceptors in arthropods.

Neurosecretory fibres in the median eyes of the scorpion, Androctonus australis L.

SummaryThe retina of the median eyes of the North African scorpion, Androctonus australis L., is supplied with numerous neurosecretory nerve fibres which establish synaptoid contacts on the retinula cells. The number of fibres or profiles of varicosities of fibre terminals associated with a retinular unit (five retinula cells with a fused rhabdom) varies between 10 and 20. Electron-opaque vesicles with a diameter of 80–100 nm are abundant within the axonal profiles. The synaptoid junctions are characterized by postsynaptic electron-dense material on the inner leaflet of the retinula cell membrane and, frequently, presynaptic submembranous dense material. Because of these ultrastructural features, the junctions observed here resemble typical interneuronal synaptic contacts. Hence this kind of neurosecretory junction appears to be unique among arthropods.It is suggested that the neurosecretory fibres within the retina represent the efferent pathways for the control of the circadian pigment movements within the retinula cells.

Staining in the brain of Pachymorpha sexguttata mediated by an antibody against a Drosophila clock-gene product: labeling of cells with possible importance for the beetle’s circadian rhythms

Abstract.Central nervous system ganglia within the head of the beetle Pachymorpha sexguttata were labeled using an antibody that recognizes an evolutionarily conserved region of the period (per) gene product of Drosophila melanogaster. per and the protein it encodes (PER) are believed to play a central role in the generation of endogenous circadian rhythms in flies; therefore anti-PER-mediated immunoreactivity may help to uncover cellular components of the circadian clock system in that insect and in others. In the beetle, application of this antibody led to the staining of a distinct set of neurons located in the optic lobes and the central brain, plus small numbers of putative glial cells in the optic lobes. Neuronal perikarya (including their nuclei in a few cases), the axons, and terminal regions of the neurons were stained. The network formed by these labeled cells and processes are candidates for the neuronal basis of the beetle’s circadian clock system: the pacemaker region situated next to the medulla neuropil, its connection to the apparent site of Zeitgeber input, and putative efferent pathways projecting to control centers of various effector systems. Anti-PER-mediated labeling and that resulting from application to beetle specimens of an antiserum against pigment-dispersing hormone (PDH) were compared; in the Drosophila brain all ’’PDH cells’’ express the per gene as well. In the beetle, however, the set of ’’PER cells’’ and PDH ones is at least in part nonoverlapping. The hypothesis that neurons stained by application of anti-PER participate in the control of the beetle’s circadian rhythms is discussed in the context of previous electrophysiological and immunohistochemical studies. Also considered are analogies to, and differences from, labeling of the PER protein in fruit flies and PER-like immunoreactivity in other animals.

Neurosecretory cells in the circadian-clock system of the scorpion, Androctonus australis.

SummaryThe somata of the efferent neurosecretory fibers that control the circadian sensitivity rhythm in the median eyes of the scorpion, Androctonus australis, were detected in the brain by retrograde labeling with Lucifer Yellow CH. A total of 20–40 neurons are arranged in two groups displaying a bilaterally symmetrical, marginal position near the circumesophageal connectives. Half the cells in each group send fibers into the ipsilateral optic nerve; the fibers from the other half enter the contralateral optic nerve.

The lateral eyes of the scorpion, Androctonus australis

SummaryThe dioptric apparatus of the lateral eyes of the scorpion, Androctonus austrails, consists of a cuticular lens, but lacks a vitreous body. The retina is formed by (1) retinula cells displaying a contiguous network of rhabdoms; (2) arhabdomeric cells bearing a distal dendrite that contacts retinula cells via numerous projections and ends before the rhabdomere of the retinula cells; (3) pigment cells that ensheath retinula and arhabdomeric cells with the exception of the contact regions; and (4) neurosecretory fibres possibly originating in the supraesophageal ganglion. The ratio of the number of retinula to arhabdomeric cells is determined to be close to 2 ∶ 1 in the three larger anterolateral eyes, in contrast to the median eyes where the ratio is 5 ∶ 1.The construction of the dioptric apparatus as well as the anatomy of the retina imply that in the lateral eyes of Androctonus australis visual acuity is reduced. A certain degree of spatial discrimination, however, may be retained by the presence of a relatively high number of arhabdomeric cells. It is suggested that the lateral eyes of A. australis mainly function as light detectors, e.g., for Zeitgeber stimuli.

Factors Affecting Date of Implantation, Parturition, and Den Entry Estimated from Activity and Body Temperature in Free-Ranging Brown Bears

Knowledge of factors influencing the timing of reproduction is important for animal conservation and management. Brown bears (Ursus arctos) are able to vary the birth date of their cubs in response to their fat stores, but little information is available about the timing of implantation and parturition in free-ranging brown bears. Body temperature and activity of pregnant brown bears is higher during the gestation period than during the rest of hibernation and drops at parturition. We compared mean daily body temperature and activity levels of pregnant and nonpregnant females during preimplantation, gestation, and lactation. Additionally we tested whether age, litter size, primiparity, environmental conditions, and the start of hibernation influence the timing of parturition. The mean date of implantation was 1 December (SD = 12), the mean date of parturition was 26 January (SD = 12), and the mean duration of the gestation period was 56 days (SD = 2). The body temperature of pregnant females was higher during the gestation and lactation periods than that of nonpregnant bears. The body temperature of pregnant females decreased during the gestation period. Activity recordings were also used to determine the date of parturition. The parturition dates calculated with activity and body temperature data did not differ significantly and were the same in 50% of the females. Older females started hibernation earlier. The start of hibernation was earlier during years with favorable environmental conditions. Dates of parturition were later during years with good environmental conditions which was unexpected. We suggest that free-ranging pregnant brown bears in areas with high levels of human activities at the beginning of the denning period, as in our study area, might prioritize investing energy in early denning than in early parturition during years with favorable environmental conditions, as a strategy to prevent disturbances caused by human.