The relationship of ocular morphology to feeding modes and activity periods in shallow marine teleosts from New Zealand

Synopsis Thirty one species of shallow water teleosts were captured from the NE coast of New Zealand. Ocular morphology was assessed in terms of eye size, pupil shape, theoretical sensitivity and acuity based on retinal morphology, and regional distribution of photoreceptors within the retina. Eye size was relatively or absolutely larger in carnivores than herbivores. Diurnal planktivores and nocturnal species of small body size maximise vision by having relatively large eyes. Anterior aphakic spaces were present in most of the species examined, and 25% of the species also had posterior aphakic spaces. Theoretical sensitivity was generally higher among nocturnal than diurnal species, however, a number of benthic and pelagic carnivores showed retinal specialization for enhanced sensitivity. Diurnal species displayed high spatial acuity, with maximum acuity occurring in carnivorous species. Crepuscular species had either high or low acuity, whereas that of nocturnal species was generally lower than in diurnal species. Ten species displayed regional variation in rod density, with crepuscular and nocturnal species showing streaks of high rod density in the retina. Eleven species of carnivores displayed regional variation in cone density, with highest density usually occurring in the caudal part of the retina. In most of the species with areas of high cone density, there was a forward visual axis that coincided with the location of the aphakic space, suggestive of accomodation along that axis.     

The eyes of a patrolling butterfly: visual field and eye structure in the Orange Sulphur, Colias eurytheme (Lepidoptera, Pieridae)

Sensory information plays a critical role in determining an animal's behavior on both proximate and evolutionary timescales. Butterflies, like many other insects, use vision extensively over their lifetimes, and yet relatively little work has been published to date on their visual capabilities. We describe the visual system of a pierid butterfly, Colias eurytheme, with the ultimate goal of better understanding its role in shaping the behavior of this animal. We made several measurements: visual field dimensions, eye surface area, interommatidial angle (Deltaphi), facet diameter (D), and eye parameter (p). C. eurytheme had a large visual field and considerable regional variation in visual acuity, as inferred by Deltaphi and D. When compared to females, males had larger eye surface areas, smaller Deltaphi, and larger D in all regions except ventrally. Both sexes had proportionally large eye surface areas compared to other butterflies. Minimum p in males was small, indicating that some regions of their eyes may operate close to the diffraction limit. Finally, we found that both eye surface area and D scaled positively, but with negative allometry to body size. We discuss the relevance of these visual characteristics to the biology and behavior of C. eurytheme.     

The finely defined shift work schedule of dung beetles and their eye morphology

In nature, nothing is wasted, not even waste. Dung, composed of metabolic trash and leftovers of food, is a high‐quality resource and the object of fierce competition. Over 800 dung beetle species (Scarabaeinae) compete in the South African dung habitat and more than 100 species can colonize a single dung pat. To coexist in the same space, using the same food, beetles divide the day between them. However, detailed diel activity periods and associated morphological adaptations have been largely overlooked in these dung‐loving insects. To address this, we used a high‐frequency trapping design to establish the diel activity period of 44 dung beetle species in their South Africa communities. This allowed us to conclude that the dung beetles show a highly refined temporal partitioning strategy, with differences in peak of activity even within the diurnal, crepuscular, and nocturnal guilds, independent of nesting behavior and taxonomic classification. We further analyzed differences in eye and body size of our 44 model species and describe their variability in external eye morphology. In general, nocturnal species are bigger than crepuscular and diurnal species, and as expected, the absolute and relative eye size is greatest in nocturnal species, followed by crepuscular and then diurnal species. A more surprising finding was that corneal structure (smooth or facetted) is influenced by the activity period of the species, appearing flat in the nocturnal species and highly curved in the diurnal species. The role of the canthus—a cuticular structure that partially or completely divides the dung beetle eye into dorsal and ventral parts—remains a mystery, but the large number of species investigated in this study nevertheless allowed us to reject any correlation between its presence and the nesting behavior or time of activity of the beetles.     

Evolution of eye size and shape in primates

Strepsirrhine and haplorhine primates exhibit highly derived features of the visual system that distinguish them from most other mammals. Comparative data link the evolution of these visual specializations to the sequential acquisition of nocturnal visual predation in the primate stem lineage and diurnal visual predation in the anthropoid stem lineage. However, it is unclear to what extent these shifts in primate visual ecology were accompanied by changes in eye size and shape. Here we investigate the evolution of primate eye morphology using a comparative study of a large sample of mammalian eyes. Our analysis shows that primates differ from other mammals in having large eyes relative to body size and that anthropoids exhibit unusually small corneas relative to eye size and body size. The large eyes of basal primates probably evolved to improve visual acuity while maintaining high sensitivity in a nocturnal context. The reduced corneal sizes of anthropoids reflect reductions in the size of the dioptric apparatus as a means of increasing posterior nodal distance to improve visual acuity. These data support the conclusion that the origin of anthropoids was associated with a change in eye shape to improve visual acuity in the context of a diurnal predatory habitus.     

Cool habitats support darker and bigger butterflies in Australian tropical forests

Morphology mediates the relationship between an organism's body temperature and its environment. Dark organisms, for example, tend to absorb heat more quickly than lighter individuals, which could influence their responses to temperature. Therefore, temperature‐related traits such as morphology may affect patterns of species abundance, richness, and community assembly across a broad range of spatial scales. In this study, we examined variation in color lightness and body size within butterfly communities across hot and cool habitats in the tropical woodland–rainforest ecosystems of northeast Queensland, Australia. Using thermal imaging, we documented the absorption of solar radiation relative to color lightness and wingspan and then built a phylogenetic tree based on available sequences to analyze the effects of habitat on these traits within a phylogenetic framework. In general, darker and larger individuals were more prevalent in cool, closed‐canopy rainforests than in immediately adjacent and hotter open woodlands. In addition, darker and larger butterflies preferred to be active in the shade and during crepuscular hours, while lighter and smaller butterflies were more active in the sun and midday hours—a pattern that held after correcting for phylogeny. Our ex situ experiment supported field observations that dark and large butterflies heated up faster than light and small butterflies under standardized environmental conditions. Our results show a thermal consequence of butterfly morphology across habitats and how environmental factors at a microhabitat scale may affect the distribution of species based on these traits. Furthermore, this study highlights how butterfly species might differentially respond to warming based on ecophysiological traits and how thermal refuges might emerge at microclimatic and habitat scales.     

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.     

Optical parameters of euphausiid eyes as a function of habitat depth

Summary The relationships between habitat depth, eye diameter relative to body length, and the dimensions of rhabdoms and crystalline cones have been examined for 13 species of three oceanic euphausiid genera with habitats ranging from near-surface waters to the deep-sea. Rate of eye growth decreases with depth. Longer rhabdoms may increase the visual sensitivity to point and extended light sources by an eye of a particular size with depth. Larger interommatidial angles suggest that visual acuity decreases at depth. Depth-related changes in euphausiid eyes are considered with respect to the probable roles of vision and bioluminescence in the deep-sea. Unusual features of the eyes of several species are described.     

EXPERIMENTAL ANALYSES OF WING SIZE,FLIGHT, AND SURVIVAL IN THE WESTERN WHITE BUTTERFLY

Butterflies have distinctively large wings relative to body size, but the functional and fitness consequences of wing size for butterflies are largely unknown. I use natural and experimentally generated variation in wing surface area to examine how decreased wing size affects flight and survival in a population of the western white butterfly, Pontia occidentalis. In the laboratory, experimental reductions in wing area (reduced-wings manipulation) significantly increased wingbeat frequencies of hovering butterflies, whereas a control manipulation had no detectable effects. In contrast, behavioral observations and mark-release-recapture (MRR) studies in the field detected no significant differences in flight activity, initial dispersal rates, or recapture probabilities among treatment groups. Estimated selection coefficients indicated that natural variation in wing size, body mass, and wing loading in the population were not significantly correlated with survival in the two MRR studies. In two mark-recapture studies with manipulated butterflies, survival probabilities were not significantly different for reduced-wings individuals compared with control or unmanipulated individuals. In summary, experimental reductions in wing area significantly altered aspects of flight in the laboratory, but did not detectably alter flight or survival in the field for this population. The large wing size typical of butterflies may reduce the functional and survival consequences of wing size variation within populations.     

Nestedness of butterfly assemblages in the Zhoushan Archipelago,China: area effects,life-history traits and conservation implications

The nested subset pattern (nestedness) of faunal assemblages has been a research focus in the fields of island biogeography and conservation biology in recent decades. However, relatively few studies have described nestedness in butterfly assemblages in oceanic archipelago systems. Moreover, previous studies often quantified nestedness using inappropriate nestedness metrics and random fill algorithms with high Type I errors. The aims of this study are to examine the existence of nestedness and underlying causal mechanisms of butterfly assemblages in the Zhoushan Archipelago, China. We used the line-transect method to determine butterfly occupancy and abundance on 42 study islands from July to August 2014. We obtained butterfly life-history traits (wingspan, body weight and minimum area requirement) by field work and island geographical features (area and isolation) from the literature. We used the recently developed metric WNODF to estimate nestedness. Partial Spearman rank correlation was used to evaluate the associations of nestedness and island geographical features as well as butterfly life-history traits related to species extinction risk and colonization ability. The butterfly assemblages were significantly nested. Island area and minimum area requirement of butterflies were significantly correlated with nestedness after controlling for other independent variables. In contrast, the nestedness of butterflies did not appear to result from passive sampling or selective colonization. However, multi-year studies are needed to confirm that target effects are not muddling these results. Our results indicate that selective extinction may be the main driver of nestedness of butterfly assemblages in our study system. From a conservation viewpoint, we should protect both large islands and species with large area requirement to maximize the number of species preserved.     

舟山群岛蝶类群落嵌套分布格局及其影响因素

片断化生境中群落的物种组成常呈现嵌套分布格局。2013年7-8月, 我们在浙江舟山群岛采用截线法对28个岛屿上的蝴蝶群落进行了野外调查, 探讨了岛屿物种嵌套分布格局及其影响因素。通过测量采集标本获得蝶类的生活史特征(最小需求面积、翅展和体重), 查阅文献资料获得蝶类的栖息地特征(岛屿面积、距最近大陆距离和距最近大岛距离), 分析了影响蝶类群落嵌套结构的因素。研究结果显示: (1)舟山群岛蝶类群落符合嵌套分布格局; (2)岛屿面积和物种最小需求面积对嵌套格局的形成有显著影响; (3)舟山群岛蝶类群落嵌套格局的形成支持选择性灭绝假说; (4)随机检验零模型结果显示该嵌套分布格局并非采样偏差造成的。因此, 在制定舟山群岛区域蝶类保护措施时, 应优先考虑那些分布在面积较大岛屿的和最小需求面积较大的物种。     

Thermoregulatory significance of wing melanization in Pieris butterflies (Lepidoptera: Pieridae): physics,posture, and pattern

Summary Pieris butterflies use a novel behavioral posture for thermoregulation called reflectance basking, in which the wings are used as solar reflectors to reflect radiation to the body. As a means of exploring the thermoregulatory significance of wing melanization patterns, I examine the relation of basking posture and wing color pattern to body temperature. A mathematical model of the reflectance process predicts certain combinations of dorsal wing melanization pattern and basking posture that maximize body temperature. Laboratory experiments and field observations show that this model correctly predicts qualitative differences in the relation of body temperature to basking posture based on differences in the extent of dorsal melanization on the wing margins, both between species and between sexes within species of Pieris. This is the first demonstration in insects that coloration of the entire wing surface can affect thermoregulation. Model and experimental results suggest that, in certain wing regions, increased melanization can reduce body temperature in Pieris; this effect of melanization is exactly the opposite of that found in other Pierid butterflies that use their wings as solar absorbers. These results are discussed in terms of the evolution of wing melanization pattern and thermoregulatory behavior in butterflies.     

Variation in compound eye structure: effects of diet and family

Studies of compound eyes have revealed that variation in eye structure can substantially affect visual performance. Here, we investigate the degree to which a stressful rearing environment, which decreases body size, affects the eye phenotype. Full siblings of the Orange Sulphur butterfly, Colias eurytheme, were collected from known parents and split within families among two diet treatments that varied in quality. In both sexes, individuals reared on the high-quality diet had larger eye height and anterior facet diameter, and therefore, by inference, superior vision. However, relative to their reduced body size, individuals reared on low-quality diet had proportionally larger eyes and facets than individuals reared on high-quality diet. We interpret this finding as evidence that butterflies encountering nutritional stress increased proportional investment in eye development to reduce loss of visual performance. We also found significant broad-sense genetic variation underlying eye structure in both males and females, and report novel heritability estimates for eye height and facet diameter. Surprisingly, there was greater genetic variation in eye height among males than among females, despite apparently stronger directional selection on male vision. We discuss the implications of these data for our understanding of eye development and evolution.     

Eye shape and activity pattern in birds

Many aspects of an animal's ecology are associated with activity pattern, the time of day when that animal is awake and active. There are two major activity patterns: diurnal , active during the day in a light-rich, or photopic, environment, and nocturnal , active after sunset in a light-limited, or scotopic, environment. Birds are also cathemeral , or equally likely to be awake at any time of day, or crepuscular , awake and active at dawn and dusk. Each of these activity patterns is associated with different levels of ambient light. This study examines how the morphology (size and shape) of the eye varies according to these different light environments for birds in a phylogenetic context. Activity pattern has a significant influence on eye shape and size in birds. Birds that are adapted for scotopic vision have eye shapes that are optimized for visual sensitivity, with larger corneal diameters relative to axial lengths. Birds that are adapted for photopic vision have eye shapes that are optimized for visual acuity, with larger axial lengths relative to corneal diameters. Birds adapted for scotopic vision also exhibit absolutely larger corneal diameters and axial lengths than do photopic birds. The results indicate that the light level under which the bird functions has a more significant influence on eye shape than phylogeny.     

Latitudinal patterns in the size of European butterflies

The importance of seasonality in shaping latitudinal size patterns was investigated in 16 species of lycaenine and satyrine butterflies with distributions in Sweden and continental Europe. Species without shifts in voltinism within the study area generally displayed clear size clines, increasing in size from north to south within Sweden. These species were also larger in continental Europe than in Sweden. In northern temperate areas a linear model for mean size at different latitudes seems to be a reasonable approximation for most species in this category. The size patterns for three species with shifts from univoltinism to bivoltinism at latitudes within Sweden were more reminiscent of the "saw-tooth"-pattern predicted by theory for such cases. The results suggest that size patterns in European butterflies to a large extent is governed by the length of the favorable season at different latitudes, affecting selection for development time and size. Altitude and drought also affect the effective season length and may amplify or complicate latitudinal patterns.     

Effects of activity pattern on eye size and orbital aperture size in primates

Among primates, nocturnal species exhibit relatively larger orbital apertures than diurnal species. Most researchers have considered this disparity in orbital aperture size to reflect differences in eye size, with nocturnal primates having relatively large eyes in order to maximize visual sensitivity. Presumed changes in eye size due to shifts in activity pattern are an integral part of theoretical explanations for many derived features of anthropoids, including highly convergent orbits and a postorbital septum. Here I show that despite clear differences in relative orbital aperture size, many diurnal and nocturnal primates do not differ in relative eye size. Among nocturnal primates, relative eye size is influenced by diet. Nocturnal visual predators (e.g., Tarsius, Loris, and Galago moholi) tend to have larger relative eye sizes than diurnal primates. By contrast, nocturnal frugivores (e.g., Perodicticus, Nycticebus, and Cheirogaleus) have relative eye sizes that are comparable to those of diurnal primates. Although some variation in orbital aperture size can be attributed to variation in eye size, both cornea size and orbit orientation also exert a strong influence on orbital aperture size. These findings argue for caution in the use of relative orbital aperture size as an indicator of activity pattern in fossil primates. These findings further suggest that existing scenarios for the evolution of unique orbital morphologies in anthropoids must be modified to reflect the importance of ecological variables other than activity pattern.     

Sex and Caste-Specific Variation in Compound Eye Morphology of Five Honeybee Species

Ranging from dwarfs to giants, the species of honeybees show remarkable differences in body size that have placed evolutionary constrains on the size of sensory organs and the brain. Colonies comprise three adult phenotypes, drones and two female castes, the reproductive queen and sterile workers. The phenotypes differ with respect to tasks and thus selection pressures which additionally constrain the shape of sensory systems. In a first step to explore the variability and interaction between species size-limitations and sex and caste-specific selection pressures in sensory and neural structures in honeybees, we compared eye size, ommatidia number and distribution of facet lens diameters in drones, queens and workers of five species (Apis andreniformis, A. florea, A. dorsata, A. mellifera, A. cerana). In these species, male and female eyes show a consistent sex-specific organization with respect to eye size and regional specialization of facet diameters. Drones possess distinctly enlarged eyes with large dorsal facets. Aside from these general patterns, we found signs of unique adaptations in eyes of A. florea and A. dorsata drones. In both species, drone eyes are disproportionately enlarged. In A. dorsata the increased eye size results from enlarged facets, a likely adaptation to crepuscular mating flights. In contrast, the relative enlargement of A. florea drone eyes results from an increase in ommatidia number, suggesting strong selection for high spatial resolution. Comparison of eye morphology and published mating flight times indicates a correlation between overall light sensitivity and species-specific mating flight times. The correlation suggests an important role of ambient light intensities in the regulation of species-specific mating flight times and the evolution of the visual system. Our study further deepens insights into visual adaptations within the genus Apis and opens up future perspectives for research to better understand the timing mechanisms and sensory physiology of mating related signals.     

Acceptance angles of butterfly ommatidia

The ommatidial acceptance angle (angular sensitivity) of seven species of butterflies was determined by a novel technique. Measurements were based upon the fact that light adaptation produces a graded contraction of specific retinula cells with a concomitant reduction in the brillance of the observed reflection (glow). Measurements were, therefore, based upon the changes in the intensity of the reflections as an adapting light was moved to various spatial positions. Measurements were also made on the angle of illumination that would produce reflections, as well as the angle through which reflections could be observed. Average angles so determined were: half-linear sensitivity, 1°16′; reflection (acceptance), 2°47′; reflection (viewing), 9–10°; inter-ommatidial, 1°47′. These results suggest that the butterfly eye may have greater acuity than those of previously studied insects.     

Conservative whole‐organ scaling contrasts with highly labile suborgan scaling differences among compound eyes of closely related Formica ants

Static allometries determine how organ size scales in relation to body mass. The extent to which these allometric relationships are free to evolve, and how they differ among closely related species, has been debated extensively and remains unclear; changes in intercept appear common, but changes in slope are far rarer. Here, we compare the scaling relationships that govern the structure of compound eyes of four closely related ant species from the genus Formica. Comparison among these species revealed changes in intercept but not slope in the allometric scaling relationships governing eye area, facet number, and mean facet diameter. Moreover, the scaling between facet diameter and number was conserved across all four species. In contrast, facet diameters from distinct regions of the compound eye differed in both intercept and slope within a single species and when comparing homologous regions among species. Thus, even when species are conservative in the scaling of whole organs, they can differ substantially in regional scaling within organs. This, at least partly, explains how species can produce organs that adhere to genus wide scaling relationships while still being able to invest differentially in particular regions of organs to produce specific features that match their ecology.     

Large‐sized insects show stronger seasonality than small‐sized ones: a case study of fruit‐feeding butterflies

Animal species have a restricted period during the year when conditions for development are optimal, and this is known as the temporal window. Duration of the temporal window can vary among species, although the causes of variation are still poorly understood. In the present study, examining butterflies, we assume that the temporal window duration is correlated with the seasonal period of flight (termed seasonality). To understand how species characteristics are correlated with this, we examine whether there is a relationship between body size and length of flight period of fruit‐feeding butterflies in forest fragments, and whether these two parameters have a phylogenetic signal. Using wing size as a measure of body size and the period of adult flight as a measure of seasonality, we found significant positive correlations between body size and seasonality among subfamilies but not within subfamilies. We also found a clear phylogenetic signal in size but not in seasonality. The results obtained suggest the existence of a trade‐off between insect size and seasonality, with size limiting flight period length. The relationship between body size and seasonality and the synchrony with their resources may be one factor explaining the vulnerability of large insects to forest fragmentation. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 820–827.     

Compound Eye Miniaturization in Lepidoptera: a comparative morphological analysis

Superposition and apposition compound eyes are commonly associated with moths and butterflies, respectively. However, recently intermediate eye designs, combining features of both apposition and superposition eyes were found in tiny insects. Here, we examine the eyes of 12 species of moth, ranging from 1.88 to 6.03 mm body size, by scanning and transmission electron microscopy. Correlations between body and eye sizes are discussed with regard to the eyes' functionality. Although all of the species shared an ommatidial organization characteristic of pterygote insects, three optical designs were found: (a) an apposition eye, (b) an eye resembling apposition eyes, but with a unique crystalline cone, and (c) an eye intermediate in structure between apposition and superposition eyes. Our comparisons also revealed a new type of basal matrix for the Lepidoptera. The results show that in most of the examined compound eyes (with the exception of the apposition eye of Micropterix aruncella), a clear distinction between apposition and superposition eyes is not feasible. Due to functional morphological constraints as a consequence of miniaturization, evolutionary transformations from superposition into apposition optics may have occurred several times independently in various ‘microlepidopteran’ taxa. The Phyllonorycter medicaginella eye appears to illustrate this evolutionary scenario best.