The evolution of bird migration—a synthesis

We approach the problem of the evolution of bird migration by asking whether migration evolves towards new breeding areas or towards survival areas in the non-breeding season. Thus, we avoid the ambiguity of the usually discussed “southern-home-theory” or “northern-home-theory”. We argue that migration evolved in birds that spread to seasonal habitats through gradual dispersal to enhance survival during the non-breeding season; this in contrast to the alternative idea suggesting that migration evolved towards new breeding areas to increase reproductive success. Our synthesis is based on the threshold model explaining how migratory traits can change rapidly through microevolutionary processes. Our model brings former theories together and explains how bird migration, with the appropriate direction and time program, evolves through selection after genetically non-directed events such as dispersal and colonization. The model does not need the former untested assumptions such as competition as a reason for migration and for the disappearance of sedentary populations or higher reproductive success in temperate breeding areas. Our theory offers answers to questions such as how birds with a southern origin may gradually reach northern latitudes, why migration routes may follow historical expansion routes and why birds leave an area for the non-breeding season and move back instead of breeding on their wintering grounds. The theory proposes gradual change through selection and not sudden changes such as long distance dispersal or mutations and can be applied to migration at all latitudes and in all directions. The scenario provides a reasonable concept to understand most of the existing migratory phenomena on the basis of the ecology and genetics of migratory behaviour.     

The eyes of oilbirds (<Emphasis Type="Italic">Steatornis caripensis</Emphasis>): pushing at the limits of sensitivity

An extreme example of a low light-level lifestyle among flying birds is provided by the oilbird, Steatornis caripensis (Steatornithidae, Caprimulgiformes). Oilbirds breed and roost in caves, often at sufficient depth that no daylight can penetrate, and forage for fruits at night. Using standard microscopy techniques we investigated the retinal structure of oilbird eyes and used an ophthalmoscopic reflex technique to determine the parameters of these birds visual fields. The retina is dominated by small rod receptors (diameter 1.3±0.2 m; length 18.6±0.6 m) arranged in a banked structure that is unique among terrestrial vertebrates. This arrangement achieves a photoreceptor density that is the highest so far recorded (1,000,000 rods mm^–2) in any vertebrate eye. Cone photoreceptors are, however, present in low numbers. The eye is relatively small (axial length 16.1±0.2 mm) with a maximum pupil diameter of 9.0±0.0 mm, achieving a light-gathering capacity that is the highest recorded in a bird (f-number 1.07). The binocular field has a maximum width of 38° and extends vertically through 100° with the bill projecting towards the lower periphery; a topography that suggests that vision is not used to control bill position. We propose that oilbird eyes are at one end of the continuum that juxtaposes the conflicting fundamental visual capacities of sensitivity and resolution. Thus, while oilbird visual sensitivity may be close to a maximum, visual resolution must be low. This explains why these birds employ other sensory cues, including olfaction and echolocation, in the control of their behaviour in low-light-level environments.     

Evolution of a new sense for wind in flying phasmids? Afferents and interneurons

The evolution of winged stick insects (phasmids) from secondarily wingless ancestors was proposed in recent studies. We explored the cuticle of flying phasmids for wind sensors that could be involved in their flight control, comparable to those known for locusts. Surprisingly, wind-sensitive hairs (wsH) occur on the palps of mouthparts and on the antennae of the winged phasmid Sipyloidea sipylus which can fly in tethered position only when air currents blow over the mouthparts. The present study describes the morphology and major functional properties of these “new” wsH with soft and bulging hair bases which are different from the beaker-like hair bases of the wsH on the cerci of phasmids and the wsH described in other insects. The most sensitive wsH of antennae and palps respond with phasic-tonic afferents to air currents exceeding 0.2 ms⁻¹. The fields of wsH on one side of the animal respond mainly to ventral, lateral, and frontal wind on the ipsilateral side of the head. Afferent inputs from the wsH converge but also diverge to a group of specific interneurons at their branches in the suboesophageal ganglion and can send their integrated input from wsH fields of the palps and antennae to the thoracic central nervous system. Response types of individual wsH-interneurons are either phasic or phasic-tonic to air puffs or constant air currents and also, the receptive fields of individual interneurons differ. We conclude that the “new” wsH system and its interneurons mainly serve to maintain flight activity in airborne phasmids and also, the “new” wsH must have emerged together with the integrating interneurons during the evolution from wingless to the recent winged forms of phasmids.     

Microspectrophotometric evidence for cone monochromacy in sharks

Sharks are apex predators, and their evolutionary success is in part due to an impressive array of sensory systems, including vision. The eyes of sharks are well developed and function over a wide range of light levels. However, whilst close relatives of the sharks—the rays and chimaeras—are known to have the potential for colour vision, an evolutionary trait thought to provide distinct survival advantages, evidence for colour vision in sharks remains equivocal. Using single-receptor microspectrophotometry, we measured the absorbance spectra of visual pigments located in the retinal photoreceptors of 17 species of shark. We show that, while the spectral tuning of the rod (wavelength of maximum absorbance, λ_max 484–518 nm) and cone (λ_max 532–561 nm) visual pigments varies between species, each shark has only a single long-wavelength-sensitive cone type. This suggests that sharks may be cone monochromats and, therefore, potentially colour blind. Whilst cone monochromacy on land is rare, it may be a common strategy in the marine environment: many aquatic mammals (whales, dolphins and seals) also possess only a single, green-sensitive cone type. It appears that both sharks and marine mammals may have arrived at the same visual design by convergent evolution. The spectral tuning of the rod and cone pigments of sharks is also discussed in relation to their visual ecology.     

Magnetoreception in birds: no intensity window in “fixed direction” responses

Under 502 nm turquoise light combined with 590 nm yellow light and in total darkness, European robins, Erithacus rubecula, no longer prefer their migratory direction, but exhibit so-called fixed direction responses that do not show the seasonal change between spring and autumn. We tested robins under these light conditions in the local geomagnetic field of 46 μT, a field of twice this intensity, 92 μT, and a field of three times this intensity, 138 μT. Under all three magnetic conditions, the birds preferred the same easterly direction under turquoise-and-yellow light and the same northwesterly direction under dark, while they were oriented in their seasonally appropriate direction under control conditions. “Fixed direction” responses are thus not limited to a narrow intensity window as has been found for normal compass orientation. This can be attributed to their origin in the magnetite-based receptor in the upper beak, which operates according to fundamentally different principles than the radical pair mechanism in the retina mediating compass orientation. “Fixed direction” responses are possibly a relict of a receptor mechanism that changed its function, now mainly providing information on magnetic intensity.     

What’s the buzz? Ultrasonic and sonic warning signals in caterpillars of the great peacock moth (Saturnia pyri)

Caterpillars have many natural enemies and, therefore, have evolved a diversity of antipredator strategies. Most research focuses on those strategies (crypsis, countershading, and warning coloration) targeting visually guided predators. In contrast, defensive sounds, although documented for more than a century, have been poorly studied. We report on a novel form of sound production—chirping—in caterpillars of the common European Great Peacock moth (Saturnia pyri). Chirps are broadband, with dominant peaks ranging between the sonic (3.7 kHz) and ultrasonic (55.1 kHz) and are generated by a rapid succession of mandibular “tooth strikes.” Chirp trains are induced by simulated predator attacks and precede or accompany the secretion of a defensive chemical from integumental bristles, supporting our hypothesis that these sounds function in acoustic aposematism. We propose that these caterpillars generate multimodal warning signals (visual, chemical, and acoustic) to target the dominant sensory modalities of different predators, including birds, bats, and invertebrates. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

How do water striders, Aquarius paludum, react to brackish water simulated by NaCl solutions?

Several stages, from eggs to adults, of the water strider, Aquarius paludum (Fabricius), inhabiting fresh water are sometimes conveyed by heavy flow in the rainy or typhoon seasons in Japan to lotic brackish water in the mouth of rivers. The water striders might then respond to salinity either by remaining to wait for extensive rainfall to reduce osmotic pressure locally before reproducing (“breed here and later tactic”) or by flying away to reproduce in fresh waters elsewhere (“breed elsewhere and later tactic”). All first instars died before the first molt when they were exposed to 1.75 and 3.5% NaCl solutions in a laboratory experiment. Living on 0.5 and 0.9% solutions through larval and adult stages slowed down larval growth and suppressed female reproduction. When exposed to the 0.5 and 0.9% solutions, 90 and 92% of males, respectively, showed histolysis of their flight muscles. Therefore, in brackish natural habitats, larvae and adults seem to follow the strategy “breed here and later.” When water striders were exposed to 0.9% solution either just after emergence or 20 days later, females showed a higher flight propensity than those kept on fresh waters throughout, and they delayed the deposition of eggs. Therefore, when conveyed to brackish water after emergence by stream flow after heavy rain, adults seem to leave the area by flight, demonstrating the strategy “breed elsewhere and later” tactic. We conclude that water striders use alternative tactics for responding to salinity, depending on the stage of exposure.     

Cold winter temperatures condition the egg-hatching dynamics of a grape disease vector

The leafhopper Scaphoideus titanus is the vector of a major phytoplasma grapevine disease, Flavescence dorée. The vector’s distribution is in Eastern and Northern Europe, and its population dynamics varies as a function of vineyard latitude. We tested the hypothesis that hatching dynamics are cued by cold temperatures observed in winter. We exposed eggs from a natural population to simulated “cold” and “mild” winters and varied the exposure time at 5 °C from 0 to 63 days. We show that temperature cooling mainly affected the onset of hatching and is negatively correlated to the cold time exposure. The majority of hatchings occurred more quickly in cold rather than in mild winter simulated conditions, but there was no significant difference between the duration of hatching of eggs whatever the cold time exposure. In agreement with the Northern American origin of the vector, the diapause termination and thus the timing regulation of egg hatching require cold winters.     

Provenancing of archeological pumice finds from North Sinai

Seven pumice samples from excavations in North Sinai have been investigated with respect to their geochemical composition. This type of volcanic rock has been used as an abrasive and thus has been an object of trade since antiquity. With the help of Instrumental Neutron Activation Analysis, six of these Bronze Age samples could be correlated to their volcanic sources on the islands of Santorini, Nisyros and Giali (Greece) using the typical element concentrations (“chemical fingerprint”). The source of one pumice sample remains unidentified excluding, however, the Santorini eruption as a possible source. The concluding section of this article discusses the possible contribution, however indirect, of the pumice from Sinai and elsewhere in the Eastern Mediterranean to the controversial issue of the accurate date of the “Minoan” eruption of Santorini.     

Histological,chemical, and morphological reexamination of the “heart” of a small Late Cretaceous <Emphasis Type="BoldItalic">Thescelosaurus</Emphasis>

A three-dimensional, iron-cemented structure found in the anterior thoracic cavity of articulated Thescelosaurus skeletal remains was hypothesized to be the fossilized remains of the animal’s four-chambered heart. This was important because the finding could be interpreted to support a hypothesis that non-avian dinosaurs were endothermic. Mammals and birds, the only extant organisms with four-chambered hearts and single aortae, are endotherms. The hypothesis that this Thescelosaurus has a preserved heart was controversial, and therefore, we reexamined it using higher-resolution computed tomography, paleohistological examination, X-ray diffraction analysis, X-ray photoelectron spectroscopy, and scanning electron microscopy. This suite of analyses allows for detailed morphological and chemical examination beyond what was provided in the original work. Neither the more detailed examination of the gross morphology and orientation of the thoracic “heart” nor the microstructural studies supported the hypothesis that the structure was a heart. The more advanced computed tomography showed the same three areas of low density as the earlier studies with no evidence of additional low-density areas as might be expected from examinations of an ex situ ostrich heart. Microstructural examination of a fragment taken from the “heart” was consistent with cemented sand grains, and no chemical signal consistent with a biological origin was detected. However, small patches of cell-like microstructures were preserved in the sandstone matrix of the thoracic structure. A possible biological origin for these microstructures is the focus of ongoing investigation.     

Nuptial feeding of spermless spermatophores in the Hawaiian swordtail cricket, Laupala pacifica (Gryllidae: Triginodiinae)

Crickets in the genus Laupala (subfamily Trigonidiinae) have an elaborate courtship system, defined by a highly ritualized serial transfer of multiple spermatophores. Males produce multiple “micro” spermatophores followed by a final “macro” spermatophore during a single mating bout. Remarkably, the microspermatophores of L. cerasina, the first species whose mating system was studied in detail, were discovered to be spermless. However, in a study of another species, L. pacifica, sperm transfer was reported after every copulation suggesting that L. pacifica microspermatophores contain sperm. The presence or absence of sperm in the microspermatophore has important implications for the evolution of this exaggerated courtship system and the origin of nuptial gifts. In this study, we systematically examined L. pacifica spermatophore contents for sperm using a fluorescent nuclear stain. We detected sperm only in macrospermatophores. This finding suggests that spermless microspermatophores are typical for Laupala; thus, to determine the origin of this highly modified phenotype will require comparative analyses with closely related outgroups that exhibit less exaggerated courtship systems.     

Extremophiles: from abyssal to terrestrial ecosystems and possibly beyond

The anthropocentric term “extremophile” was introduced more than 30 years ago to describe any organism capable of living and growing under extreme conditions—i.e., particularly hostile to human and to the majority of the known microorganisms as far as temperature, pH, and salinity parameters are concerned. With the further development of studies on microbial ecology and taxonomy, more “extreme” environments were found and more extremophiles were described. Today, many different extremophiles have been isolated from habitats characterized by hydrostatic pressure, aridity, radiations, elevated temperatures, extreme pH values, high salt concentrations, and high solvent/metal concentrations, and it is well documented that these microorganisms are capable of thriving under extreme conditions better than any other organism living on Earth. Extremophiles have also been investigated as far as the search for life in other planets is concerned and even to evaluate the hypothesis that life on Earth came originally from space. Extremophiles are interesting for basic and applied sciences. Particularly fascinating are their structural and physiological features allowing them to stand extremely selective environmental conditions. These properties are often due to specific biomolecules (DNA, lipids, enzymes, osmolites, etc.) that have been studied for years as novel sources for biotechnological applications. In some cases (DNA polymerase, thermostable enzymes), the search was successful and the final application was achieved, but certainly further exploitations are next to come.     

Female feeding regime and polyandry in the nuptially feeding nursery web spider, Pisaura mirabilis

We examined the influence of female feeding regime on polyandry in the nuptially feeding nursery web spider (Pisaura mirabilis). In this species, the nuptial gift, a dead prey item wrapped in the male’s silk, is physically separate from the ejaculate. We manipulated female feeding regime (starved or fed) and the presence or absence of a gift with three successive males to test direct-benefits hypotheses (nuptial gift or sperm supply) for the expression of polyandry. The presence of a gift was necessary for copulation, as no male without a gift successfully copulated. Female mating behavior most strongly supports polyandry due to the accumulation of gifted food items (“nuptial gift” direct-benefits hypothesis). Starved females that were presented with a gift accepted significantly more gifts and inseminations than fed females. Most starved females (74%) copulated two or more times, as opposed to only 3% of the fed females. Nearly all of the females that accepted a gift subsequently copulated. The nuptial gift item seems to function as male mating effort and females appear to receive multiple matings as part of a feeding strategy.     

Birds,berries and UV

The problem of UV vision in vertebrates is briefly discussed in its historical context. For example, UV vision has been demonstrated in some birds by several authors. Hence the reflectances of plumage, petals of bird-pollinated flowers and of berries in the near UV may play an important rôle within the visual environment of birds. Some data obtained by means of UV photography are presented, and it is shown, that the waxlayer of glaucous fruits is highly reflective in the UV.     

Experience,but not distance,influences the recruitment precision in the stingless bee <Emphasis Type="Italic">Scaptotrigona mexicana</Emphasis>

Recruitment precision, i.e. the proportion of recruits that reach an advertised food source, is a crucial adaptation of social bees to their environment. Studies with honeybees showed that recruitment precision is not a fixed feature, but it may be enhanced by factors like experience and distance. However, little is known regarding the recruitment precision of stingless bees. Hence, in this study, we examined the effects of experience and spatial distance on the precision of the food communication system of the stingless bee Scaptotrigona mexicana. We conducted the experiments by training bees to a three-dimensional artificial patch at several distances from the colony. We recorded the choices of individual recruited foragers, either being newcomers (foragers without experience with the advertised food source) or experienced (foragers that had previously visited the feeder). We found that the average precision of newcomers (95.6 ± 2.61%) was significantly higher than that of experienced bees (80.2 ± 1.12%). While this might seem counter-intuitive on first sight, this “loss” of precision can be explained by the tendency of experienced recruits to explore nearby areas to find new rewarding food sources after they had initially learned the exact location of the food source. Increasing the distance from the colony had no significant effect on the precision of the foraging bees. Thus, our data show that experience, but not the distance of the food source, affected the patch precision of S. mexicana foragers.     

Representation of complex visual stimuli in the brain

A method was developed to investigate transfer properties of neurons in the visual system using pictures of complex visual stimuli. The picture is moved over the receptive field of a neuron so that it can scan it along programmed lines. The activity of the neuron during the scanning procedure is presented in a two-dimensional dot display on scale with the original picture. By superposition of the stimulus and the transfer pattern, one can find out to which detail of a stimulus the neuron responds. Neurons in the first intracerebral relay of the visual system, the lateral geniculate body, reduce a complex stimulus, such as a photograph of a natural environment, to its contours. Cortical cells only respond to contours either of a limited or of a wider range of orientations (simple and complex cells, respectively). But the course of contours is only described by a continuous representation of these contours in the cortical map of the visual field. This is done by the simple cells, which have small receptive fields and thus a higher resolving power, whereas complex cells with their large receptive fields monitor the approximate location of a moving stimulus. The function of these two classes of neurons is discussed in terms of visual behavior, i.e., for fixation, hold, and binocular vergence movements (simple cells), and for detection of moving objects and motor command signals towards these objects (complex cells). These functions are an important condition for foveal vision which is the basis of perception in primates. An important function of orientation sensitivity of simple cells may be the binocular alignment of contours in binocular fusion and stereoscopic vision.     

Regional,seasonal and interspecific variation in <Superscript>15</Superscript>N and <Superscript>13</Superscript>C in sympatric mouse lemurs

Madagascar provides some of the rare examples where two or more primate species of the same genus and with seemingly identical niche requirements occur in sympatry. If congeneric primate species co-occur in other parts of the world, they differ in size in a way that is consistent with Hutchinson’s rule for coexisting species, or they occupy different ecological niches. In some areas of Madagascar, mouse lemurs do not follow these “rules” and thus seem to violate one of the principles of community ecology. In order to understand the mechanisms that allow coexistence of sympatric congeneric species without obvious niche differentiation, we studied food composition of two identical sized omnivorous mouse lemur species, Microcebus griseorufus and M. murinus with the help of stable isotope analyses (δ ¹⁵N and δ ¹³C). The two species are closely related sister species. During the rich season, when food seems abundant, the two species do not differ in their nitrogen isotope composition, indicating that the two species occupy the same trophic level. But they differ in their δ ¹³C values, indicating that M. griseorufus feeds more on C₄ and CAM (Crassulacean-acid-metabolism) plants than M. murinus. During the lean season, M. murinus has lower δ ¹⁵N values, indicating that the two species feed at different trophic levels during times of food shortage. Hybrids between the two species showed intermediate food composition. The results reflect subtle differences in foraging or metabolic adaptations that are difficult to quantify by traditional observations but that represent possibilities to allow coexistence of species.     

Public acceptance and risk-benefit perception of CO<Subscript>2</Subscript> geological storage for global warming mitigation in Japan

CO₂ geological storage will be one of the cost-effective options for global warming mitigation, and this technology is under development widely in the world. However, the technology may face the challenge of public acceptance before its implementation. In order to evaluate the public acceptance, questionnaire surveys were conducted among Japanese university students. A cognitive map of geological storage, together with other major global warming mitigation options, everyday life activities, etc., was constructed by means of a statistical analysis of the responses to the questionnaire. The risk-benefit cognitive map consists of the following factors: “risk perception,” “benefit perception,” and “public acceptance.” The risk perception is further disaggregated into “dread risk” and “unknown risk.” Additionally, a second survey was conducted after providing the students with additional information on global warming and CO₂ geological storage, and the effects of the information on their perceptions were evaluated. The effects of risk and benefit perceptions on public acceptance were evaluated and discussed based on the cognitive maps representing the perceptions before and after providing the information. The analyses revealed that the benefit perception was more influential than the risk perception on the public acceptance of CO₂ geological storage. The benefit perception increased greatly after providing the information; however, the unknown risk remained considerably large. Further, RD&D relating unknown risk, for example, the monitoring technology for stored CO₂ and the risk assessment of CO₂ leakage, and the supply of related information to the public would be beneficial for increasing the public acceptance.     

A bee in the corridor: centering and wall-following

In an attempt to better understand the mechanism underlying lateral collision avoidance in flying insects, we trained honeybees (Apis mellifera) to fly through a large (95-cm wide) flight tunnel. We found that, depending on the entrance and feeder positions, honeybees would either center along the corridor midline or fly along one wall. Bees kept following one wall even when a major (150-cm long) part of the opposite wall was removed. These findings cannot be accounted for by the “optic flow balance” hypothesis that has been put forward to explain the typical bees’ “centering response” observed in narrower corridors. Both centering and wall-following behaviors are well accounted for, however, by a control scheme called the lateral optic flow regulator, i.e., a feedback system that strives to maintain the unilateral optic flow constant. The power of this control scheme is that it would allow the bee to guide itself visually in a corridor without having to measure its speed or distance from the walls.