Behavioural environments and niche construction: the evolution of dim-light foraging in bees

Most bees forage for floral resources during the day, but temporal patterns of foraging activity vary extensively, and foraging in dim-light environments has evolved repeatedly. Facultative dim-light foraging behaviour is known in five of nine families of bees, while obligate behaviour is known in four families and evolved independently at least 19 times. The light intensity under which bees forage varies by a factor of 10⁸, and therefore the evolution of dim-light foraging represents the invasion of a new, extreme niche. The repeated evolution of dim-light foraging behaviour in bees allows tests of the hypothesis that behaviour acts as an evolutionary pacemaker. With the exception of one species of Apis , facultative dim-light foragers show no external structural traits that are thought to enable visually mediated flight behaviour in low-light environments. By contrast, most obligate dim-light foragers show a suite of convergent optical traits such as enlarged ocelli and compound eyes. In one intensively studied species ( Megalopta genalis ) these optical changes are associated with neurobiological changes to enhance photon capture. The available ecological evidence suggests that an escape from competition for pollen and nectar resources and avoidance of natural enemies are driving factors in the evolution of obligate dim-light foraging.     

The evolution of nocturnal behaviour in sweat bees,Megalopta genalis and M. ecuadoria (Hymenoptera: Halictidae): an escape from competitors and enemies?

Evolutionary transitions to dim-light foraging (predawn matinal, crepuscular, nocturnal) have occurred repeatedly in bees, and may be associated with an escape from enemies or competitors. To date, however, little information has been available to test these hypotheses. Here we provide the first detailed information on the nesting behaviour of two species of Neotropical, nocturnal sweat bees, Megalopta genalis and M. ecuadoria (Hymenoptera: Halictidae). Females are facultatively social or solitary, and construct nests in dead wood. Nocturnal foraging behaviour is bimodal. Bees began foraging after sunset (∼18:30 h) and ceased foraging approximately 1 h later even though nocturnal flowers with pollen were still abundant; a second foraging bout occurred in the predawn morning, which began at ∼04:45 h and ended around sunrise (∼06:15 h) when diurnal-blooming flowers were abundant. Bees are capable of controlled flight in full light. They utilized pollen from both canopy and understory plant species, which have diurnal or nocturnal pollen anthesis. Megalopta nests are attacked by generalist predators such as ants, as well as the endoparasitic fly Melaloncha sp. nov. (Phoridae), the beetle Macrosaigon gracilis (Rhipophoridae), the parasitic wasp Lophostigma cincta (Mutillidae), and the brood parasite Megalopta byroni (Halictidae). Overall nest survivorship rates were comparable to those for diurnal relatives, but rates of cell parasitism for Megalopta (< < 5%) were substantially lower than they are for day-flying relatives, offering some support for the hypothesis that the evolution of nocturnal behaviour enables escape from natural enemies.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 83 , 377–387.     

Visual reliability and information rate in the retina of a nocturnal bee

Nocturnal animals relying on vision typically have eyes that are optically and morphologically adapted for both increased sensitivity and greater information capacity in dim light. Here, we investigate whether adaptations for increased sensitivity also are found in their photoreceptors by using closely related and fast-flying nocturnal and diurnal bees as model animals. The nocturnal bee Megalopta genalis is capable of foraging and homing by using visually discriminated landmarks at starlight intensities. Megalopta's near relative, Lasioglossum leucozonium, performs these tasks only in bright sunshine. By recording intracellular responses to Gaussian white-noise stimuli, we show that photoreceptors in Megalopta actually code less information at most light levels than those in Lasioglossum. However, as in several other nocturnal arthropods, Megalopta's photoreceptors possess a much greater gain of transduction, indicating that nocturnal photoreceptors trade information capacity for sensitivity. By sacrificing photoreceptor signal-to-noise ratio and information capacity in dim light for an increased gain and, thus, an increased sensitivity, this strategy can benefit nocturnal insects that use neural summation to improve visual reliability at night.     

Visual ecology of Indian carpenter bees I: Light intensities and flight activity

Bees are mostly active during the daytime, but nocturnality has been reported in some bee families. We studied temporal flight activity in three species of carpenter bees (genus Xylocopa) in relation to light intensities. X. leucothorax is diurnal, X. tenuiscapa is largely diurnal being only occasionally crepuscular, while X. tranquebarica is truly nocturnal. Occasional forays into dim light by X. tenuiscapa are likely to be due to the availability of richly rewarding Heterophragma quadriloculare (Bignoniaceae) flowers, which open at night. X. tranquebarica can fly even during the moonless parts of nights when light intensities were lower than 10⁻⁵ cd m⁻², which makes this species the only truly nocturnal bee known so far. Other known dim-light species fly during crepuscular or moonlit periods. We compare eye and body sizes with other known diurnal and dim-light bees. We conclude that while extremely large ocellar diameters, large eye size:body size ratio, large number of ommatidia and large ommatidial diameters are all adaptations to dim-light foraging, these alone do not sufficiently explain the flights of X. tranquebarica in extremely dim light. We hypothesise that additional adaptations must confer extreme nocturnality in X. tranquebarica.     

Tropical pollinators in the canopy and understory: Field data and theory for stratum “preferences”

Claims have been made for a canopy preference by large bees pollinating tropical flowers—without data or tests that support or refute this opinion. The working hypothesis for bee foraging behavior in three dimensions is that forager experience can produce stratum fidelity, just as rewarding foraging produces floral fidelity. Wideranging search behavior should allow bees to track spatiotemporal distribution of resources. A systematic study of 20 bee species and 10 genera: Apis, Trigona, Eulaema, Centris, Euglossa, Scaptotrigona, Partamona, Megalopta, Rhinetula,and Oxytrigonawas made in two forests in Panama. Two traps were operated simultaneously at canopy height and in the understory to test whether there were consistent stratum associations. Studies were continuous for 1 and 8 years. The only high-canopy foragers were two nocturnal bees, all the rest flew at both heights with similar probability or consistently came to lower traps. Large euglossines showed a tendency to forage high, which was directly related to their capacity for heat loss during flight, compared to smaller euglossines. They are also more conspicuous in warning coloration, another expected correlate of foraging more often in the open. Although large variance in stratum association predominates, some medium-sized diurnal forest bees avoid the exposed upper canopy, while some nocturnal bees tend to forage there.     

Nocturnal vision and landmark orientation in a tropical halictid bee

BACKGROUND: Some bees and wasps have evolved nocturnal behavior, presumably to exploit night-flowering plants or avoid predators. Like their day-active relatives, they have apposition compound eyes, a design usually found in diurnal insects. The insensitive optics of apposition eyes are not well suited for nocturnal vision. How well then do nocturnal bees and wasps see? What optical and neural adaptations have they evolved for nocturnal vision? RESULTS: We studied female tropical nocturnal sweat bees (Megalopta genalis) and discovered that they are able to learn landmarks around their nest entrance prior to nocturnal foraging trips and to use them to locate the nest upon return. The morphology and optics of the eye, and the physiological properties of the photoreceptors, have evolved to give Megalopta's eyes almost 30 times greater sensitivity to light than the eyes of diurnal worker honeybees, but this alone does not explain their nocturnal visual behavior. This implies that sensitivity is improved by a strategy of photon summation in time and in space, the latter of which requires the presence of specialized cells that laterally connect ommatidia into groups. First-order interneurons, with significantly wider lateral branching than those found in diurnal bees, have been identified in the first optic ganglion (the lamina ganglionaris) of Megalopta's optic lobe. We believe that these cells have the potential to mediate spatial summation. CONCLUSIONS: Despite the scarcity of photons, Megalopta is able to visually orient to landmarks at night in a dark forest understory, an ability permitted by unusually sensitive apposition eyes and neural photon summation.     

Recreated Ancestral Opsin Associated with Marine to Freshwater Croaker Invasion Reveals Kinetic and Spectral Adaptation

Rhodopsin, the light-sensitive visual pigment expressed in rod photoreceptors, is specialized for vision in dim-light environments. Aquatic environments are particularly challenging for vision due to the spectrally dependent attenuation of light, which can differ greatly in marine and freshwater systems. Among fish lineages that have successfully colonized freshwater habitats from ancestrally marine environments, croakers are known as highly visual benthic predators. In this study, we isolate rhodopsins from a diversity of freshwater and marine croakers and find that strong positive selection in rhodopsin is associated with a marine to freshwater transition in South American croakers. In order to determine if this is accompanied by significant shifts in visual abilities, we resurrected ancestral rhodopsin sequences and tested the experimental properties of ancestral pigments bracketing this transition using in vitro spectroscopic assays. We found the ancestral freshwater croaker rhodopsin is redshifted relative to its marine ancestor, with mutations that recapitulate ancestral amino acid changes along this transitional branch resulting in faster kinetics that are likely to be associated with more rapid dark adaptation. This could be advantageous in freshwater due to the redshifted spectrum and relatively narrow interface and frequent transitions between bright and dim-light environments. This study is the first to experimentally demonstrate that positively selected substitutions in ancestral visual pigments alter protein function to freshwater visual environments following a transition from an ancestrally marine state and provides insight into the molecular mechanisms underlying some of the physiological changes associated with this major habitat transition.     

The Evolution and Expression of the Moth Visual Opsin Family

Because visual genes likely evolved in response to their ambient photic environment, the dichotomy between closely related nocturnal moths and diurnal butterflies forms an ideal basis for investigating their evolution. To investigate whether the visual genes of moths are associated with nocturnal dim-light environments or not, we cloned long-wavelength (R), blue (B) and ultraviolet (UV) opsin genes from 12 species of wild-captured moths and examined their evolutionary functions. Strong purifying selection appeared to constrain the functions of the genes. Dark-treatment altered the levels of mRNA expression in Helicoverpa armigera such that R and UV opsins were up-regulated after dark-treatment, the latter faster than the former. In contrast, B opsins were not significantly up-regulated. Diel changes of opsin mRNA levels in both wild-captured and lab-reared individuals showed no significant fluctuation within the same group. However, the former group had significantly elevated levels of expression compared with the latter. Consequently, environmental conditions appeared to affect the patterns of expression. These findings and the proportional expression of opsins suggested that moths potentially possessed color vision and the visual system played a more important role in the ecology of moths than previously appreciated. This aspect did not differ much from that of diurnal butterflies.     

Juvenile hormone levels in honey bee (Apis mellifera L.) foragers: foraging experience and diurnal variation

A rising blood titer of juvenile hormone (JH) in adult worker honey bees is associated with the shift from working in the hive to foraging. We determined whether the JH increase occurs in anticipation of foraging or whether it is a result of actual foraging experience and/or diurnal changes in exposure to sunlight. We recorded all foraging flights of tagged bees observed at a feeder in a large outdoor flight cage. We measured JH from bees that had taken 1, 3-5, or >100 foraging flights and foragers of indeterminate experience leaving or entering the hive. To study diurnal variation in JH, we sampled foragers every 6h over one day. Titers of JH in foragers were high relative to nurses as in previous studies, suggesting that conditions in the flight cage had no effect on the relationship between foraging behavior and JH. Titers of JH in foragers showed no significant effects of foraging experience, but did show significant diurnal variation. Our results indicate that the high titer of JH in foragers anticipates the onset of foraging and is not affected by foraging experience, but is modulated diurnally.     

Comparative Analysis of Japanese Three-Spined Stickleback Clades Reveals the Pacific Ocean Lineage Has Adapted to Freshwater Environments while the Japan Sea Has Not

Divergent selection and adaptive divergence can increase phenotypic diversification amongst populations and lineages. Yet adaptive divergence between different environments, habitats or niches does not occur in all lineages. For example, the colonization of freshwater environments by ancestral marine species has triggered adaptive radiation and phenotypic diversification in some taxa but not in others. Studying closely related lineages differing in their ability to diversify is an excellent means of understanding the factors promoting and constraining adaptive evolution. A well-known example of the evolution of increased phenotypic diversification following freshwater colonization is the three-spined stickleback. Two closely related stickleback lineages, the Pacific Ocean and the Japan Sea occur in Japan. However, Japanese freshwater stickleback populations are derived from the Pacific Ocean lineage only, suggesting the Japan Sea lineage is unable to colonize freshwater. Using stable isotope data and trophic morphology, we first show higher rates of phenotypic and ecological diversification between marine and freshwater populations within the Pacific Ocean lineage, confirming adaptive divergence has occurred between the two lineages and within the Pacific Ocean lineage but not in the Japan Sea lineage. We further identified consistent divergence in diet and foraging behaviour between marine forms from each lineage, confirming Pacific Ocean marine sticklebacks, from which all Japanese freshwater populations are derived, are better adapted to freshwater environments than Japan Sea sticklebacks. We suggest adaptive divergence between ancestral marine populations may have played a role in constraining phenotypic diversification and adaptive evolution in Japanese sticklebacks.     

Effects of recent experience on foraging decisions by bumble bees

The temporal and spatial scales employed by foraging bees in sampling their environment and making foraging decisions should depend both on the limits of bumble bee memory and on the spatial and temporal pattern of rewards in the habitat. We analyzed data from previous experiments to determine how recent foraging experience by bumble bees affects their flight distances to subsequent flowers. A single visit to a flower as sufficient to affect the flight distance to the next flower. However, longer sequences of two or three visits had an additional effect on the subsequent flight distance of individual foragers. This suggests that bumble bees can integrate information from at least three flowers for making a subsequent foraging decision. The existence of memory for floral characteristics at least at this scale may have significance for floral selection in natural environments.     

Light intensity limits foraging activity in nocturnal and crepuscular bees

A crepuscular or nocturnal lifestyle has evolved in bees severaltimes independently, probably to explore rewarding pollen sourceswithout competition and to minimize predation and nest parasites.Despite these obvious advantages, only few bee species are nocturnal.Here we show that the sensitivity of the bee apposition eyeis a major factor limiting the ability to forage in dim light.We present data on eye size, foraging times, and light levelsfor Megalopta genalis (Augochlorini, Halictidae) in Panama,and Lasioglossum (Sphecodogastra) sp. (Halictini, Halictidae)in Utah, USA. M. genalis females forage exclusively during twilight,but as a result of dim light levels in the rain forest, theyare adapted to extremely low intensities. The likely factorlimiting their foraging activity is finding their nest entranceon return from a foraging trip. The lowest light intensity atwhich they can do this, both in the morning and the evening,is 0.0001 cd m^–2. Therefore, they leave the nest at dimmerlight levels in the morning than in the evening. Lasioglossum(Sphecodogastra) foraging is limited by light intensity in theevening, but probably by temperature in the morning in the temperateclimate of Utah. We propose that the evolution of nocturnalityin bees was favored by the large variance in the size of females.     

Retinal and optical adaptations for nocturnal vision in the halictid bee<Emphasis Type="Italic"> Megalopta genalis</Emphasis>

The apposition compound eye of a nocturnal bee, the halictid Megalopta genalis, is described for the first time. Compared to the compound eye of the worker honeybee Apis mellifera and the diurnal halictid bee Lasioglossum leucozonium, the eye of M. genalis shows specific retinal and optical adaptations for vision in dim light. The major anatomical adaptations within the eye of the nocturnal bee are (1) nearly twofold larger ommatidial facets and (2) a 4–5 times wider rhabdom diameter than found in the diurnal bees studied. Optically, the apposition eye of M. genalis is 27 times more sensitive to light than the eyes of the diurnal bees. This increased optical sensitivity represents a clear optical adaptation to low light intensities. Although this unique nocturnal apposition eye has a greatly improved ability to catch light, a 27-fold increase in sensitivity alone cannot account for nocturnal vision at light intensities that are 8 log units dimmer than during daytime. New evidence suggests that additional neuronal spatial summation within the first optic ganglion, the lamina, is involved.B.G. is thankful for travel awards from the Royal Physiographic Society, the Per Westlings Fond, the Foundation of Dagny and Eilert Ekvall and the Royal Swedish Academy of Sciences. E.J.W. is grateful for the support of a Smithsonian Short-Term Research Fellowship, the Swedish Research Council, the Crafoord Foundation, the Wenner-Gren Foundation and the Royal Physiographic Society of Lund for their ongoing support     

Rhodopsin population genetics and local adaptation: variable dim-light vision in sand gobies is illuminated

The visual pigments of fish are thought to be adapted to the variable spectral qualities of aquatic light environments. Most research on the role of natural selection on the evolution of rhodopsins and dim-light vision in fish has focused on variation among species and higher taxa. In this issue, Larmuseau et al. reveal substantial intraspecific sequence variation in RH1 (the rhodopsin gene) in sand gobies ( Pomatoschistus minutus ). Using population genetics and molecular evolution approaches, they detect positive selection on RH1 and find evidence for adaptation to local light conditions.     

Evolution of visual pigments in geckos

Most geckos are nocturnal forms and possess rod retinas, but some diurnal genera have pure-cone retinas. We isolated cDNAs encoding the diurnal gecko opsins, dg1 and dg2, similar to nocturnal gecko P521 and P467, respectively. Despite the large morphological differences between the diurnal and nocturnal gecko photoreceptor types, they express phylogenetically closely related opsins. These results provide molecular evidence for the reverse transmutation, that is, rods of an ancestral nocturnal gecko have backed into cones of diurnal geckos. The amino acid substitution rates of dgl and dg2 are higher than those of P521 and P467, respectively. Changes of behavior regarding photic environment may have contributed to acceleration of amino acid substitutions in the diurnal gecko opsins.     

Allometry and resolution of bee eyes (Apoidea)

A sample of compound eyes from 15 species of female pollen foraging bees (apiform Apoidea) was morphometrically analyzed. These species were chosen for size differences, different social organization, and a wide geographic and taxonomic distribution (Apidae, Megachilidae, Andrenidae, Halictidae). The results demonstrate the following characteristics for the typical compound eye in female foraging bees: (1) the vertical diameter of the eye is about twice the horizontal diameter; (2) the eyes of diurnal foragers scale isometrically with body size; (3) the eyes of three species of nocturnal foragers have about 1.8 times the surface area as compared to diurnal foragers of matching size; (4) the number of ommatidia per eye range from about 1000 in Perdita minima to about 16 000 in Xylocopa latipes; and (5) the corresponding mean interommatidial angles range from 4.7 to 1.2 degrees . Body size, rather than species-specific ecological adaptation, is the major (97%) determinant of the number of ommatidia per eye in diurnal, as well as nocturnal foragers. The number of ommatidia per eye, and hence the visual resolution, is proportional to the square root of both body size and eye size across all species studied. The eye parameter (the product of the mean interommatidial angle and the mean lens diameter) increases slightly with decreasing body size. All this is taken as evidence that the features of the bees' visual macro-niche remained largely constant over the roughly 130 million years of their macro-evolution.     

夜行性昆虫微光视觉行为及其视觉适应机制

作为昆虫种群的重要组成部分,夜行性昆虫成功进化出了与其生存环境相适应的感觉机制,普遍认为夜行性昆虫主要依靠嗅觉和机械性感受等来探索环境,其视觉器官发生了退化或功能丧失.近年来,随着红外夜视、视网膜电位(electroretinogram,ERG)和视觉神经等生物新技术的应用,昆虫视觉生态学研究出现了突破性进展,自200...     

Physiological variation as a mechanism for developmental caste-biasing in a facultatively eusocial sweat bee

Social castes of eusocial insects may have arisen through an evolutionary modification of an ancestral reproductive ground plan, such that some adults emerge from development physiologically primed to specialize on reproduction (queens) and others on maternal care expressed as allo-maternal behaviour (workers). This hypothesis predicts that variation in reproductive physiology should emerge from ontogeny and underlie division of labour. To test these predictions, we identified physiological links to division of labour in a facultatively eusocial sweat bee, Megalopta genalis. Queens are larger, have larger ovaries and have higher vitellogenin titres than workers. We then compared queens and workers with their solitary counterparts-solitary reproductive females and dispersing nest foundresses-to investigate physiological variation as a factor in caste evolution. Within dyads, body size and ovary development were the best predictors of behavioural class. Queens and dispersers are larger, with larger ovaries than their solitary counterparts. Finally, we raised bees in social isolation to investigate the influence of ontogeny on physiological variation. Body size and ovary development among isolated females were highly variable, and linked to differences in vitellogenin titres. As these are key physiological predictors of social caste, our results provide evidence for developmental caste-biasing in a facultatively eusocial bee.     

木蜂的访花行为和传粉作用

木蜂作为蜜蜂科的重要类群,是热带和亚热带地区显花植物常见的传粉者.木蜂具有访花的季节时间长、访花植物种类多、能耐高温或低光照、能嗡声传粉等特点.这些访花特点是木蜂作为热带植物、尤其是温室作物、夜间开花植物和部分茄属植物的重要传粉者.近年来国外已经证明木蜂能有效为蓝莓、西番莲、荷包豆、温室西红柿和温室甜瓜授粉,但我国有关木蜂为多数农作物传粉的重要性和有效性的证据较少.本文综述了近年来木蜂的访花行为和传粉作用的研究进展,为进一步保护、管理和利用木蜂资源提供理论依据.     

Behavioral rhythmicity, age, division of labor and period expression in the honey bee brain.

Young adult honey bees work inside the beehive "nursing" brood around the clock with no circadian rhythms; older bees forage for nectar and pollen outside with strong circadian rhythms. Previous research has shown that the development of an endogenous rhythm of activity is also seen in the laboratory in a constant environment. Newly emerging bees maintained in isolation are typically arrhythmic during the first few days of adult life and develop strong circadian rhythms by about a few days of age. In addition, average daily levels of period (per) mRNA in the brain are higher in foragers or forager-age bees (> 21 days of age) relative to young nest bees (approximately 7 days of age). The authors used social manipulations to uncouple behavioral rhythmicity, age, and task to determine the relationship between these factors and per. There was no obligate link between average daily levels of per brain mRNA and either behavioral rhythmicity or age. There also were no differences in per brain mRNA levels between nurse bees and foragers in social environments that promote precocious or reversed behavioral development. Nurses and other hive-age bees can have high or low levels of per mRNA levels in the brain, depending on the social environment, while foragers and foraging-age bees always have high levels. These findings suggest a link between honey bee foraging behavior and per up-regulation. Results also suggest task-related differences in the amplitude of per mRNA oscillation in the brain, with foragers having larger diurnal fluctuation in per than nurses, regardless of age. Taken together, these results suggest that social factors may exert potent influences on the regulation of clock genes.