Infrared spectral sensitivity of Melanophila acuminata

The spectral sensitivity of the pit organ of the beetle Melanophila acuminata (Coleoptera:Buprestidae) was measured using an ultrafast tunable infrared laser source and standard electrophysiological techniques. The pit organ may be classified as a broadband detector as the beetles responded to all infrared excitation wavelengths from 2 to 6&mgr;m. There was a decrease in response threshold and latency and an increase in the magnitude of the response in the region from 2.8 to 3.5&mgr;m, which corresponded to a region of decreased transmittance (increased absorbance) as measured by Fourier transform infrared spectroscopy. The implications of the correlation between spectral response and optical properties are discussed.     

Sensitivity threshold and response characteristics of infrared detection in the beetle Melanophila acuminata (Coleoptera: Buprestidae)

The minimum detection threshold of the infrared sensitive beetle, Melanophila acuminata, was measured with a helium-neon laser that emitted light at a wavelength of 3.39 microm. Extracellular recordings were taken both at the pit organ responsible for detection and at the interganglionic connectives in the thorax of the beetle. At the pit organ, generator and action potentials from single neurons were measured with a sharpened tungsten electrode. At the connectives that linked the fused second meso-/metathoracic and prothoracic ganglia, compound action potentials were measured with a tungsten hook electrode that encircled the connective. The latter recordings confirmed conveyance of infrared information through specific pathways to rostrally-situated sites in the nervous system of the beetle. The 50% probability irradiance threshold at which action potentials were elicited from the receptor and connectives occurred at 17.3 and 14.6 mW/cm(2), respectively. In addition to sensitivity threshold, several other characteristics of the response were quantified including dependence of generator potential latency, generator potential duration, spike frequency, and spike latency on irradiance, dependence of response strength (spike count) on exposure time, and flicker fusion frequency. The ability to detect infrared radiation is rare in nature, and these results provide valuable information necessary to understand this unique sensitivity.     

The analysis of the mechanosensory origin of the infrared sensilla in Melanophila acuminata (Coeloptera; Buprestidae) adduces new insight into the transduction mechanism

The thoracic infrared (IR) sensilla of the pyrophilous jewel beetle Melanophila acuminata most likely have evolved from hair mechanoreceptors (sensilla trichodea). To further elucidate the sensory transduction mechanism, the morphology of IR sensilla and of neighbouring hair mechanoreceptors was investigated by using conventional electron microscopical techniques (SEM, TEM) in combination with focused ion beam milling (FIB). It was assumed that any deviation from the bauplan of a sensillum trichodeum is of particular concern for the transduction of IR radiation into a mechanical stimulus. Thus, the structures supposed to be relevant for stimulus uptake and transduction were homologized. Compared to a hair mechanoreceptor, an IR sensillum shows the following special features: (i) the formation of a complex cuticular sphere instead of the bristle; the sphere consists of an outer exocuticular shell as well as of an inner porous mesocuticular part. (ii) The enclosure of the dendritic tip of the mechanosensitive neuron inside the sphere in a fluid-filled inner pressure chamber which is connected with a system of microcavities and nanocanals in the mesocuticular part. Hence we propose that an IR sensillum most probably acts as a microfluidic converter of infrared radiation into an increase in internal pressure inside the sphere which is measured by the mechanosensitive neuron.     

Mechanism of Infrared Detection and Transduction by Beetle Melanophila Acuminata In memory of Jerry Wolken

The Melanophila acuminata beetle is attracted to forest fires via a pair of infrared sensory organs composed of sensilla. Our histological work showed that each sensillum contains lipid layers surrounding a protein layer and a unique polysaccharide base that is associated with a neuron to each sensillum. Infrared microscopy showed that the protein region maximally absorbs infrared radiation at 3 μm wavelength and at 10 μm, which corresponds to the known radiation produced by forest fires at 3 μm.Mathematical calculations showed that the physical properties of the sensilla are such that the expected temperature rise is insufficient for transduction of the infrared signal through mechanical means or as a thermal receptor as previously thought;hence the protein plays the pivotal role in perception of single photons and transmission of the signal within the sensilla.     

The infrared receptor of Melanophila acuminata De Geer (Coleoptera: Buprestidae): ultrastructural study of a unique insect thermoreceptor and its possible descent from a hair mechanoreceptor

The paired infrared organs of Melanophila acuminata consist of 50-100 sensilla situated at the bottom of a pit next to the coxae of the mesothoracic legs, where no exocuticle is developed. Each sensillum is accompanied by a wax gland and has a cuticular lens-like spherule (diameter 12-15 mum) bulging out with its upper hemisphere above the surface, covered only by a thin cuticle of about 1 mum. Distal processes of two enveloping cells surround the entire spherule in the form of a flattened protoplasmatic layer with the exception of a small apical stalk connecting the spherule to the outer cuticle. The spherule is innervated by a single sensory neuron of the ciliary type which is anchored ventrally with the distal tip of its cylindrical and unbranched DOS in the spherule. The insertion of the dendrite, which contains a well-developed tubular body, is always eccentric like in a hair mechanoreceptor (sensillum trichodeum) and there is no evidence of any optical function of the spherule. Three enveloping cells exist, but only one - probably the trichogen cell - forms a relatively small outer receptor lymph cavity. In the posterior wall of the pit - where exocuticle is developed - so-called suppressed systems can be found which remain completely below the cuticle with their otherwise well-developed spherules. Additionally, there is a tendency towards basally flattening and longitudinally stretching of spherules which are situated more peripherally. They strongly resemble the basal regions of hair mechanoreceptors (sensilla trichodea) in their immediate neighbourhood which are also accompanied by wax glands. Because of the existence of these transitional stages and the great ultrastructural resemblance between infrared receptors and hair mechanoreceptors concerning the bauplan of the sensory neurons and their mode of innervating the cuticular apparatus, we conclude that the infrared sensilla are probably derived from hair mechanoreceptors. Based on these results and transmission measurements of infrared radiation through the cuticular components of the organ, a model of the possible function of the infrared receptor is presented.     

The Python pit organ: imaging and immunocytochemical analysis of an extremely sensitive natural infrared detector

The Python infrared-sensitive pit organ is a natural infrared imager that combines high sensitivity, ambient temperature function, microscopic dimensions, and self-repair. We are investigating the spectral sensitivity and signal transduction process in snake infrared-sensitive neurons, neither of which is understood. For example, it is unknown whether infrared receptor neurons function on a thermal or a photic mechanism. We imaged pit organs in living Python molurus and Python regius using infrared-sensitive digital video cameras. Pit organs were significantly more absorptive and/or emissive than surrounding tissues in both 3-5 microns and 8-12 microns wavelength ranges. Pit organs exhibited greater absorption/emissivity in the 8-12 microns range than in the 3-5 microns range. To directly test the relationship between photoreceptors and pit organ infrared-sensitive neurons, we performed immunocytochemistry using antisera directed against retinal photoreceptor opsins. Retinal photoreceptors were labeled with antisera specific for retinal opsins, but these antisera failed to label terminals of infrared-sensitive neurons in the pit organ. Infrared-receptive neurons were also distinguished from retinal photoreceptors on the basis of their calcium-binding protein content. These results indicate that the pit organ absorbs infrared radiation in two major atmospheric transmission windows, one of which (8-12 microns) matches emission of targeted prey, and that infrared receptors are biochemically distinct from retinal photoreceptors. These results also provide the first identification of prospective biochemical components of infrared signal transduction in pit organ receptor neurons.     

Wide-band spectral tuning of heat receptors in the pit organ of the copperhead snake (Crotalinae)

Receptors located in the facial pit organ of certain species of snake signal the presence of prey. Infrared radiation is an effective stimulus suggesting that these receptors may be low-threshold temperature receptors. We recorded from the nerve innervating the pit organ of snakes belonging to the family of Crotalinae while stimulating the receptive area with well-defined optical stimuli. The objective was to determine the sensitivity of these receptors to a wide range (0.400-10.6 micro m) of optical stimuli to determine if a temperature-sensitive or photosensitive protein initiated signal transduction. We found that receptors in the pit organ exhibited a unique broad response to a wide range of electromagnetic radiation ranging from the near UV to the infrared. The spectral tuning of these receptors parallels closely the absorption spectra of water and oxyhemoglobin, the predominant chromophore in tissue. Our results support the hypothesis that these are receptors activated by minute temperature changes induced by direct absorption of optical radiation in the thin pit organ membrane.     

Modelling a historic oil-tank fire allows an estimation of the sensitivity of the infrared receptors in pyrophilous Melanophila beetles

Pyrophilous jewel beetles of the genus Melanophila approach forest fires and there is considerable evidence that these beetles can detect fires from great distances of more than 60 km. Because Melanophila beetles are equipped with infrared receptors and are also attracted by hot surfaces it can be concluded that these infrared receptors are used for fire detection.The sensitivity of the IR receptors is still unknown. The lowest threshold published so far is 0.6 W/m(2) which, however, cannot explain the detection of forest fires by IR radiation from distances larger than approximately 10 km. To investigate the possible sensitivity of the IR receptors we assumed that beetles use IR radiation for remote fire detection and we made use of a historic report about a big oil-tank fire in Coalinga, California, in 1924. IR emission of an oil-tank fire can be calculated by "pool fire" simulations which now are used for fire safety and risk analysis. Assuming that beetles were lured to the fire from the nearest forests 25 and 130 km away, our results show that detection from a distance of 25 km requires a threshold of the IR receptors of at least 3×10(-2) W/m(2). According to our investigations most beetles became aware of the fire from a distance of 130 km. In this case the threshold has to be 1.3×10(-4) W/m(2). Because such low IR intensities are buried in thermal noise we suggest that the infrared sensory system of Melanophila beetles utilizes stochastic resonance for the detection of weak IR radiation. Our simulations also suggest that the biological IR receptors might be even more sensitive than uncooled technical IR sensors. Thus a closer look into the mode of operation of the Melanophila IR receptors seems promising for the development of novel IR sensors.     

Afferent projections of infrared-sensitive sensilla in the beetle Melanophila acuminata (Coleoptera: Buprestidae)

Beetles of the genus Melanophila are able to detect infrared radiation by using specialized sensilla in their metathoracic pit organs. We describe the afferent projections of the infrared-sensitive neurons in the central nervous system. The axons primarily terminate in the central neuropil of the fused second thoracic ganglia where they establish putative contacts with ascending interneurons. Only a few collaterals appear to be involved in local (uniganglionic) circuits. About half of the neurons send their axons further anterior to the prothoracic ganglion. A subset of these ascend to the subesophageal ganglion, and about 10% project to the brain. Anatomical similarities suggest that the infrared-sensitive neurons are derived from neurons supplying mechanosensory sensilla. The arborization pattern of the infrared afferents suggests that infrared information is processed and integrated upstream from the thoracic ganglia.     

Thermal modeling of snake infrared reception: evidence for limited detection range

For more than 40 years, information has circulated with regard to the sensitivity of infrared pit organs in both boid and crotaline snakes (pythons and pit vipers, respectively). The most often quoted sensitivity is 0.003 degrees C and this value is based on the work of Bullock and co-workers (1956). Missing from previous work was a quantitative model of radiation transfer that would report sensitivity not in terms of degrees Celsius, but rather sensing distance. Since prey detection is often cited as the function of the infrared pit organ, quantification of this sensing distance seemed to be an important value that was missing from the literature. In this paper, we model the radiation transfer process from a 37 degrees C object, i.e. warm-blooded prey, to an infrared pit organ. The model tries to answer a very basic question-at what distance does the thermal signature of a 37 degrees C object blend into the background for a non-imaging biological infrared sensor? The output of the model, the sensing distance, is of particular interest in comparing biological infrared sensors to current semiconductor-based infrared (IR) detectors-largely because of inappropriate comparisons between the temperature sensitivity of IR snake reception and imaging IR cameras. The purpose of the presented work to make more appropriate comparisons, i.e. sensing distance. This sensing distance output indicates an extremely short detection distance (<5 cm)-contradictory to what is observed experimentally. This dichotomy raises further questions regarding how the biological system amplifies this weak signal.     

The photomechanic infrared receptor for the detection of forest fires in the beetle Melanophila acuminata (Coleoptera: Buprestidae)

We recorded from single units of individual sensilla of the thoracic infrared (IR) pit organs of Melanophila acuminata. When the organ was stimulated with a thermal radiator whose emission spectrum was similar to that of a typical forest fire, units responded phasically with up to seven spikes within 30–40 ms at a radiation power of 24 mW cm⁻². In the experiments all wavelengths shorter than 1.6 μm were excluded by a longpass IR filter. Response latencies were about 4 ms and initial impulse frequencies were up to 250 impulses per second (ips). A single spike could be generated even when stimulus duration was only 2 ms. Reduction of total radiation power from 24 mW cm⁻² to 5 mW cm⁻² resulted in increased response latencies of 5–6 ms and the occurrence of only two to three spikes. Initial impulse frequencies decreased to 125 ips. According to our physiological results and calculations, Melanophila should be able to detect a 10-hectare fire from a distance of 12 km. Mechanical stimuli also evoked responses of the IR sensilla. All present morphological and physiological findings lead to the conclusion that the IR receptors of Melanophila must function by means of a hitherto undescribed photomechanic mechanism. Accepted: 1 November 1997     

Surface ultrastructure of pit organ, spectacle, and non pit organ epidermis of infrared imaging boid snakes: A scanning probe and scanning electron microscopy study.

Boid snakes possess unique infrared imaging pit organs. The ultrastructure of the surfaces of these organs scatter or reflect electromagnetic radiation of specific wavelengths. Pit organ epidermal surfaces of boid snakes are covered with arrays of pore-like structures called micropits. In order to determine the dimensions of this complicated surface structure, we have performed the first ultrastructural analysis on snake epidermis by high-resolution microscopy techniques. Using scanning probe microscopy and scanning electron microscopy, we found that the epidermis of pit organ, maxillary non pit organ, spectacle, and ventral scales contain arrays of micropits. These scale surfaces also contain major surface features of overlapping plate-like structures. Pit organ micropits averaged 319 nm in diameter and 46 nm in depth and were spaced an average of 808 nm from each other. These micropits were significantly deeper, of greater diameter, and spaced at greater distances apart than those of the other scales. Plate structures of the pit organs had a mean distance between plates of 3.5 microm and a mean plate step height of 151 nm. These differences serve to strengthen the argument that arrays of micropit and plate surface structures function as spectral filters or anti-reflective coatings with respect to incident electromagnetic radiation.     

Reduced performance of prey targeting in pit vipers with contralaterally occluded infrared and visual senses

Both visual and infrared (IR) senses are utilized in prey targeting by pit vipers. Visual and IR inputs project to the contralateral optic tectum where they activate both multimodal and bimodal neurons. A series of ocular and pit organ occlusion experiments using the short-tailed pit viper (Gloydius brevicaudus) were conducted to investigate the role of visual and IR information during prey targeting. Compared with unoccluded controls, snakes with either both eyes or pit organs occluded performed more poorly in hunting prey although such subjects still captured prey on 75% of trials. Subjects with one eye and one pit occluded on the same side of the face performed as well as those with bilateral occlusion although these subjects showed a significant targeting angle bias toward the unoccluded side. Performance was significantly poorer when only a single eye or pit was available. Interestingly, when one eye and one pit organ were occluded on opposite sides of the face, performance was poorest, the snakes striking prey on no more than half the trials. These results indicate that, visual and infrared information are both effective in prey targeting in this species, although interference between the two modalities occurs if visual and IR information is restricted to opposite sides of the brain.     

Defensive and infrared reception responses of true vipers, pitvipers, Azemiops and colubrids

It has been suggested that true vipers (Viperidae: Viperinae) possess the ability to detect temperature differences between objects despite the lack of an apparent infrared radiation sensor. We tested the ability to distinguish between heated and unheated targets in three species of pitvipers (Viperidae: Crotalinae), four species of true vipers, two species of colubrids (Colubridae: Natricinae, Colubrinae) and Azemiops feae (Viperidae: Azemiopinae). All species of pitvipers tested could distinguish between the warm and cool targets, while no tested species of true viper, colubrid or Azemiops demonstrated this ability. In addition, pitvipers exhibited behaviors that true vipers or Azemiops did not exhibit. Our results suggest that the tested species of true vipers, Azemiops and colubrids may not posses the ability to sense infrared radiation or do not use it in a defensive context, and suggest that some defensive behaviors are associated with the pit organ in pitvipers.     

Molecular convergence of infrared vision in snakes

It has been discovered that the transient receptor potential ankyrin 1 (TRPA1) proteins of Boidae (boas), Pythonidae (pythons), and Crotalinae (pit vipers) are used to detect infrared radiation, but the molecular mechanism for detecting the infrared radiation is unknown. Here, relating the amino acid substitutions in their TRPA1 proteins and the functional differentiations, we propose that three parallel amino acid changes (L330M, Q391H, and S434T) are responsible for the development of infrared vision in the three groups of snakes. Protein modeling shows that the three amino acid changes alter the structures of the central region of their ankyrin repeats.     

Glycoproteins bound to ion channels mediate detection of electric fields: a proposed mechanism and supporting evidence

The mechanism by which animals detect weak electric and magnetic fields has not yet been elucidated. We propose that transduction of an electric field (E) occurs at the apical membrane of a specialized cell as a consequence of an interaction between the field and glycoproteins bound to the gates of ion channels. According to the model, a glycoprotein mass (M) could control the gates of ion channels, where M > 1.4 x 10(-18)/E, resulting in a signal of sufficient strength to overcome thermal noise. Using the electroreceptor organ of Kryptopterus as a mathematical and experimental model, we showed that at the frequency of maximum sensitivity (10 Hz), fields as low as 2 microV/m could be detected, and that the observation could be explained if a glycoprotein mass of 0.7 x 10(-12) kg (a sphere 11 microm in diameter) were bound to channel gates. Antibodies against apical membrane structures in Kryptopterus blocked field transduction, which was consistent with the proposal that it occurred at the membrane surface. Although the target of the field was hypothesized to be an ion channel, the proposed mechanism can easily be extended to include other kinds of membrane proteins.     

蛇类红外线感受系统:一种可能的外气功研究实验动物模型

许多蛇类,例如响尾蛇属,洞蛇属,饭匙倩蛇属,竹叶青蛇属和蝮蛇属等在头部具有一对能在黑暗中探测和捕获猎物的凹陷器官。这种凹陷器官对红外射线非常敏感,因此也称为红外线感受器官。凹陷器官在中间部位被一层约为15μm厚的薄膜(红外线感受膜)分隔为外腔和内腔,红外线感受膜由三叉神经节中的特化假单极神经细胞(红外线感受细胞)的外周轴突所支配,红外线感受膜内相邻的游离神经末梢聚合形成约40μm直径的团块,构成了基本的红外线感受野单元。三叉神经节中的红外线感受细胞的中枢轴突投射到同侧延髓中的三叉神经束外侧降核,该神经核团为此类蛇属所特有。从三叉神经束外侧降核二级神经元发出的轴突投射到对侧视顶盖。由于蛇类不具有分化的半球新皮质,因此视顶盖为红外线感受系统的感觉与行为的整合中枢。在三叉神经节,延髓三叉神经束外侧降核及视顶盖均可记录到神经细胞对红外线刺激的反应电位,从而可观察红外线刺激强度与各级红外线感受神经元反应强度的关系。本文简述了蛇类红外线感受系统的形态学和生理学特征及其研究进展,并且探讨了利用蛇类红外线感受系统作为生物体接受外气功研究的实验动物模型的可能性。     

Physical mechanism of cell number self-regulation in a population

It was shown that concentration of cells in a culture of Protozoa phylum (Infusoria) depends on cultivation volume. To explain the effect, a mechanism is proposed by which the maximum possible amount of cells in the culture is regulated. The mechanism is related to the density of radiation (electromagnetic or acoustic) flux emitted by cells. The radiation density increases with the cellularity in the cultivation volume and therefore can provide information on the total number of cells in the volume. The rations of cell concentrations in different volumes calculated under this assumption are in a good agreement with experimental data. It is proposed that a similar mechanism operates in the feed-back chain that regulates the cellularity in growing organs of multicellular organisms. It was concluded that, owing to this mechanism, mitoses during the growth of the organ would occur with increasing frequency at the periphery rather than in the center of the organ. Experimental evidence in support of this conclusion is presented.     

The dynamics of gas bubbles in conduits of vascular plants and implications for embolism repair

Pressure-induced tensions in the xylem, the water conducting tissue of vascular plants, can lead to embolism in the water-conducting cells. The details and mechanisms of embolism repair in vascular plants are still not well understood. In particular, experimental results which indicate that embolism repair may occur during xylem tension cause great problems with respect to current paradigms of plant water transport. The present paper deals with a theoretical analysis of interfacial effects at the pits (pores in the conduit walls), because it was suggested that gas-water interfaces at the pit pores may be involved in the repair process by hydraulically isolating the embolized conduit. The temporal behaviour of bubbles at the pit pores was especially studied since the question of whether these pit bubbles are able to persist is of crucial importance for the suggested mechanism to work. The results indicate that (1) the physical preconditions which are necessary for the suggested mechanism appear to be satisfied, (2) pit bubbles can achieve temporal stability and therefore persist and (3) dissolving of bubbles in the conduit lumen may lead to the final breakdown of the hydraulic isolation. The whole process is, however, complex and strongly dependent on the detailed anatomy of the pit and the contact angle.     

Tissue-Specific Expression of the β-Subunit of Tryptophan Synthase in Camptotheca acuminata, an Indole Alkaloid-Producing Plant

Camptothecin is an anticancer drug produced by the monoterpene indole alkaloid pathway in Camptotheca acuminata. As part of an investigation of the camptothecin biosynthetic pathway, we have cloned and characterized a gene from C. acuminata encoding the beta-subunit of tryptophan (Trp) synthase (TSB). In C. acuminata TSB provides Trp for both protein synthesis and indole alkaloid production and therefore represents a junction between primary and secondary metabolism. TSB mRNA and protein were detected in all C. acuminata organs examined, and their abundance paralleled that of camptothecin. Within each shoot organ, TSB was most abundant in vascular tissues. Within the root, however, TSB expression was most abundant in the outer cortex. TSB has been localized to chloroplasts in Arabidopsis, but there was little expression of TSB in C. acuminata tissues where the predominant plastids were photosynthetically competent chloroplasts. Expression of the promoter from the C. acuminata TSB gene in transgenic tobacco plants paralleled expression of the native gene in C. acuminata in all organs except roots. TSB is also highly expressed in C. acuminata during early seedling development at a stage corresponding to peak accumulation of camptothecin, consistent with the idea that Trp biosynthesis and the secondary indole alkaloid pathway are coordinately regulated.