Use of animation in teaching cell biology

To address the different learning styles of students, and because students can access animation from off-campus computers, the use of digital animation in teaching cell biology has become increasingly popular. Sample processes from cell biology that are more clearly presented in animation than in static illustrations are identified. The value of animation is evaluated on whether the process being taught involves motion, cellular location, or sequential order of numerous events. Computer programs for developing animation and animations associated with cell biology textbooks are reviewed, and links to specific examples of animation are given. Finally, future teaching tools for all fields of biology will increasingly benefit from an expansion of animation to the use of simulation. One purpose of this review is to encourage the widespread use of animations in biology teaching by discussing the nature of digital animation.     

Maternal Effect by Stem Females in <Emphasis Type="Italic">Brachionus plicatilis</Emphasis>: Effect of Starvation on Mixis Induction in Offspring

We examined whether starvation during the initial period of life in stem females affected reproductive characteristics of the offspring. Starvation treatment had different effects on rotifers hatched from resting eggs and those hatched from amictic eggs. When stem females experienced starvation after hatching, this induced a higher percentage of mixis in their offspring. When the same starvation treatment was applied to rotifers hatched from amictic eggs, there was no effect on the induction of mixis. It is probable that stem females hatched from resting eggs have specific features that are vulnerable to unfavorable environmental conditions, and that these features can be inherited by their offspring through the maternal cytoplasm.     

Growth rate, size, and sex ratio of last-laid, last-hatched offspring in the tree swallow Tachycineta bicolor

In tree swallows Tachycineta bicolor, last‐laid eggs typically hatch one to two days after the other eggs in the clutch hatch, putting last‐hatched offspring at a disadvantage when competing for food delivered by parents. We studied the biology of last‐laid, last‐hatched tree swallow offspring over two years in a Wyoming, USA, population. Our first objective was to compare the growth of last‐hatched offspring to that of their earlier‐hatched nestmates. One previous study had suggested that last‐hatched, competitively disadvantaged offspring grow feathers faster than senior nestmates, even at the expense of other aspects of growth. This may allow last‐hatched offspring to fledge with senior nestmates and avoid abandonment by parents. A second objective was to determine the sex of nestlings from last‐laid eggs. If last‐laid eggs typically produce undersized, weak adults that are poor competitors for resources, and if the fitness costs of being undersized/weak are more severe for males than for females, then selection may favour having offspring from last‐laid eggs to be female. In this study, last‐laid eggs hatched in 63 of 66 (94%) nests and hatched last in 93% of cases. At hatching, offspring from last‐laid eggs weighed, on average, 63% as much as their three heaviest nestmates (range: 26–107%). Offspring from last‐laid eggs fledged from 71% of the nests that produced at least one fledgling and apparently starved to death in remaining nests. Last‐hatched offspring who were presumably at a substantial competitive disadvantage (those whose mass at hatching was no more than about 75% of the mean mass of their three heaviest nestmates), gained mass more slowly than their senior nestmates but they eventually attained the same peak mass before fledging. Last‐hatched offspring grew primary feathers more slowly than their senior nestmates although the difference in growth rate was slight (0.2 mm/d) and only marginally significant. As a group, offspring from last‐laid eggs did not differ from offspring from all other eggs in either maximum mass attained before fledging or tarsus length at fledging. This is atypical for species with asynchronous hatching and is possibly the result of another unusual trait: the tendency of parent tree swallows to distribute food equally among young within broods. The sex ratio of offspring from last‐laid eggs did not deviate from 1:1 (22 males, 21 females). Given that last‐hatched eggs do not routinely produce undersized/weak individuals in our study population, there should be little selection on parent females to bias the sex ratio of last‐laid offspring towards females.     

Increased lifetime reproductive success of first‐hatched siblings in Common Kestrels Falco tinnunculus

Order of birth has profound consequences on offspring across taxa during development and can have effects on individuals later in life. In birds, differential maternal allocation and investment in their progeny lead to variance in the environmental conditions that offspring experience during growth within the brood. In particular, laying and hatching order have been proposed to influence individual quality during the growing period, but little is known about the fitness consequences that these two factors have for offspring from a lifetime perspective. We explored the effect of laying and hatching order on post‐fledgling survival (measured as recruitment probability) and lifetime reproductive success (LRS) in Common Kestrels Falco tinnunculus, using a long‐term and individual‐based dataset. First‐hatched chicks showed higher survival probability and LRS than their siblings. This effect was not due to body condition of the individuals at adulthood, the quality of their mates or the reproductive outcome compared with later‐hatched individuals. Instead, first‐hatched chicks had a higher recruitment probability. This could be explained by the higher body condition attained by first‐hatched chicks at the end of the nesting period, perhaps due to an enhanced competitive advantage for food over their siblings at the time of hatching. Laying order, in contrast to hatching order, appeared to have little or no effect on LRS. Our results suggest that hatching order within siblings predicts fitness, and that better early‐life conditions during growth experienced by first‐hatched chicks improve first survival and then recruitment, resulting in an enhanced LRS.     

Hatching rhythms in three species of Diclidophora (Monogenea) with observations on host behaviour.

Eggs of three species of Diclidophora were incubated in alternating 12 h periods of light and darkness at 13 degrees C. Eggs of D. merlangi collected at Arbroath hatched during the illumination period with most larvae being recovered in the first 4-6 h; some evidence of a seasonal difference in hatching of these eggs was found. Eggs of D. merlangi collected at Plymouth hatched with a peak of larval recovery in the 2 h period before the light came on. Eggs of D. luscae hatched over 'dusk' while those of D. denticulata hatched after the light was switched off. Neither mechanical disturbance nor the proximity of host tissue caused hatching in D. merlangi or D. luscae. Observations on the behaviour of the host fishes suggest that the hatching rhythms are adapted to specific host behaviour patterns.     

Feedback between size balance and consumption strongly affects the consequences of hatching phenology in size‐dependent predator–prey interactions

In many size‐dependent predator–prey systems, hatching phenology strongly affects predator–prey interaction outcomes. Early‐hatched predators can easily consume prey when they first interact because they encounter smaller prey. However, this process by itself may be insufficient to explain all predator–prey interaction outcomes over the whole interaction period because the predator–prey size balance changes dynamically throughout their ontogeny. We hypothesized that hatching phenology influences predator–prey interactions via a feedback mechanism between the predator–prey size balance and prey consumption by predators. We experimentally tested this hypothesis in an amphibian predator–prey model system. Frog tadpoles Rana pirica were exposed to a predatory salamander larva Hynobius retardatus that had hatched 5, 12, 19 or 26 days after the frog tadpoles hatched. We investigated how the salamander hatch timing affected the dynamics of prey mortality, size changes of both predator and prey, and their subsequent life history (larval period and size at metamorphosis). The predator–prey size balance favoured earlier hatched salamanders, which just after hatching could successfully consume more frog tadpoles than later hatched salamanders. The early‐hatched salamanders grew rapidly and their accelerated growth enabled them to maintain the predator‐superior size balance; thus, they continued to exert strong predation pressure on the frog tadpoles in the subsequent period. Furthermore, frog tadpoles exposed to the early‐hatched salamanders were larger at metamorphosis and had a longer larval period than other frog tadpoles. These results suggest that feedback between the predator‐superior size balance and prey consumption is a critical mechanism that strongly affects the impacts of early hatching of predators in the short‐term population dynamics and life history of the prey. Because consumption of large nutrient‐rich prey items supports the growth of predators, a similar feedback mechanism may be common and have strong impacts on phenological shifts in size‐dependent trophic relationships.     

Hatch date‐dependent differences in early growth and development recorded in the otolith microstructure of Trachurus japonicus

Otolith microstructure of 308 juvenile jack mackerel Trachurus japonicus sampled in the southern Sea of Japan between June and September 2002 were examined by light microscopy. Hatch‐date distribution indicated a protracted spawning season from 16 January to 30 May 2002. The first secondary primordium (SP) was formed at ages 19–54 days, with a mean ±  s . d . of 30·4 ± 6·1. The number of SP in an otolith ranged from two to 15, with a mean of 6·1 ± 1·7. Age of the first SP formation, number of SP and increment width varied with hatch date. In general, late‐hatched fish were younger when the first SP formed, and had a higher number of SP and wider increments, than early‐hatched fish. As increment width is a linear function of somatic growth and formation of the first SP is associated with metamorphosis in jack mackerel, these variations in otolith microstructure indicated that rates of growth (as inferred from wider increments) and development (as inferred by younger age of first SP formation) were higher in late‐hatched fish relative to early‐hatched fish. Higher temperature experienced by late‐hatched fish during early life stages may contribute critically to their higher growth and development rates compared to early‐hatched fish.     

Caenorhabditis elegans PTR/PTCHD PTR-18 promotes the clearance of extracellular hedgehog-related protein via endocytosis

Spatiotemporal restriction of signaling plays a critical role in animal development and tissue homeostasis. All stem and progenitor cells in newly hatched C. elegans larvae are quiescent and capable of suspending their development until sufficient food is supplied. Here, we show that ptr-18, which encodes the evolutionarily conserved patched-related (PTR)/patched domain-containing (PTCHD) protein, temporally restricts the availability of extracellular hedgehog-related protein to establish the capacity of progenitor cells to maintain quiescence. We found that neural progenitor cells exit from quiescence in ptr-18 mutant larvae even when hatched under starved conditions. This unwanted reactivation depended on the activity of a specific set of hedgehog-related grl genes including grl-7. Unexpectedly, neither PTR-18 nor GRL-7 were expressed in newly hatched wild-type larvae. Instead, at the late embryonic stage, both PTR-18 and GRL-7 proteins were first localized around the apical membrane of hypodermal and neural progenitor cells and subsequently targeted for lysosomal degradation before hatching. Loss of ptr-18 caused a significant delay in GRL-7 clearance, causing this protein to be retained in the extracellular space in newly hatched ptr-18 mutant larvae. Furthermore, the putative transporter activity of PTR-18 was shown to be required for the appropriate function of the protein. These findings not only uncover a previously undescribed role of PTR/PTCHD in the clearance of extracellular hedgehog-related proteins via endocytosis-mediated degradation but also illustrate that failure to temporally restrict intercellular signaling during embryogenesis can subsequently compromise post-embryonic progenitor cell function.     

Growth of yellow-headed blackbird Xanthocephalus xanthocephalus nestlings in relation to maternal body condition, egg mass, and yolk carotenoids concentrations

Condition‐dependent resource allocation to eggs can affect offspring growth and survival, with potentially different effects on male and female offspring, particularly in sexually dimorphic species. We investigated the influence of maternal body condition (i.e., mass‐tarsus residuals) and two measures of female resource allocation (i.e., egg mass, yolk carotenoid concentrations) on nestling mass and growth rates in the polygynous and highly size dimorphic yellow‐headed blackbird Xanthocephalus xanthocephalus. Egg characteristics and carotenoid concentrations were obtained from the third‐laid egg of each clutch and were correlated with the mass and growth rates of the first two asynchronously hatched nestlings. Maternal body condition was associated with the growth of first‐hatched, but not second‐hatched nestlings. Specifically, females in better body condition produced larger and faster growing first‐hatched nestlings than females in poorer body condition. As predicted for a polygynous, size‐dimorphic species, females that fledged first‐hatched sons were in better body condition than females that fledged first‐hatched daughters. Associations between egg mass, yolk carotenoid content, and nestling growth were also specific to hatching‐order. Egg mass was positively correlated with the mass and growth rates of second‐hatched nestlings, and yolk concentrations of β‐carotene were positively correlated with second‐hatched nestling mass. Surprisingly, the relationship between yolk lutein and hatchling growth differed between the sexes. Females with high concentrations of yolk lutein produced larger and faster growing first‐hatched sons, but smaller first‐hatched daughters than females with lower lutein concentrations. Mass and growth rates did not differ between first‐ and second‐hatched nestlings of the same sex, despite asynchronous hatching in the species. Results from this study suggest that maternal body condition and the allocation of resources to eggs have carotenoid‐, sex‐, and/or hatch‐order‐specific effects on yellow‐headed blackbird nestlings.     

Hatching asynchrony can have long‐term consequences for offspring fitness in zebra finches under captive conditions

Hatching asynchrony can have profound short‐term consequences for offspring, although the long‐term consequences are less well understood. The purpose of this study was to examine the long‐term consequences of hatching asynchrony for offspring fitness in birds. Specifically, we aimed to test the hypothesis that hatching asynchrony increases the sexual attractiveness and fecundity, respectively, of early‐hatched male and female zebra finch, Taeniopygia guttata (Vieillot, 1817) offspring. Mate‐choice trials comparing male nestlings with the same parents, but that were reared in asynchronous or experimentally synchronous broods, revealed no female preference in relation to hatching regime. We did however find strong evidence that, as adults, late‐hatched males were more attractive to females than siblings that had hatched earlier. Meanwhile, we found a weak trend towards early‐hatched females depositing more carotenoids and retinol in the egg yolk than late‐hatched or synchronously hatched females, although there were no differences in terms of clutch characteristics or the deposition of α‐tocopherol or γ‐tocopherol in the egg yolk. Therefore, we found that the beneficial long‐term consequences of hatching asynchrony were sex specific, being accrued by late‐hatched male nestlings and by early‐hatched female nestlings. Consequently, we conclude that the long‐term consequences of hatching asynchrony are more complex than previously realised. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106 , 430–438.     

Parental care in Semipalmated Sandpipers Calidris pusilla: brood desertion by females

Although Semipalmated Sandpipers Calidris pusilla are monogamous, with biparental incubation, most females (86–97%) deserted their broods to the care of their mates, 0–11 days (average 6) after their eggs hatched. Males left the brood an average of 8 days later, shortly before or after the chicks fledged. In several instances, females that deserted in one year remained with the chicks the next year, and vice versa. Females deserted chicks at nests that hatched later in the season at an earlier age than those had hatched earlier ( r ²> o.6). Since females appeared to have an energy deficit in at least some years, and suffered higher mortality rates than males during breeding, it is possible that females deserted broods in order to take advantage of better feeding conditions at migratory stopovers in northeastern North America early in the season. There was little evidence of higher nesting success or earlier hatching date in reuniting pairs, although if both members of a pair returned to the breeding area, 80% reunited. Increased survival of their mate may be most advantageous to males in ensuring that they obtain a female the following year.     

Approximation and visualization of large-scale motion of protein surfaces

We present a method for the approximation and real-time visualization of large-scale motion of protein surfaces. A molecular surface is represented by an expansion of spherical harmonic functions, and the motion of protein atoms around their equilibrium positions is computed by normal mode analysis. The motion of the surface is approximated by projecting the normal mode vectors of the solvent-accessible atoms to the spherical harmonic representation of the molecular surface. These surface motion vectors are represented by a separated spherical harmonic expansion. Representing the surface geometry and the surface motion vectors by spherical harmonic expansions allows variable-resolution analysis and real-time display of the large-scale surface motion. This technique has been applied to interactive visualization, interactive surface manipulation, and animation.     

Juvenile helping in the moorhen,Gallinula chloropus

In a 3-year study of the moorhen, Gallinula chloropus, some chicks from first broods stayed on their natal territory once they had reached independence, and helped to rear their younger, second brood, siblings. Juvenile dispersal was constrained by habitat saturation, and first brood young were forced to stay on their natal territory. Juveniles that hatched early in the year were forced to stay longer, and helped more than those that hatched late. The total feeding rates to broods with and without juvenile helpers were the same, but parents with helpers reduced their feeding rates relative to parents without helpers. Pairs with helpers (=pairs attempting second broods) reared more chicks per nesting, attempt than pairs rearing chicks at the same time of year without helpers (=pairs attempting first clutch renests). This was true both for all clutches, and for hatched clutches only, even when controlling for parental quality, territory size and scasonal effects.     

Survival and behavioral characteristics of amphidromous goby larvae of Sicyopterus japonicus (Tanaka, 1909) during their downstream migration

To understand the ecology and environmental tolerances of newly hatched larvae of the amphidromous fish Sicyopterus japonicus during their downstream migration, the salinity tolerance of eggs, 0-15 day old larvae, and adults, and the temperature tolerance, specific gravity and phototaxis of hatched larvae were examined. Tolerances of adults were measured as survival after a 24 h challenge in freshwater (FW), brackish water (1/3 SW) and seawater (SW). The survival rate of adult S. japonicus was 100% in FW and 1/3 SW, while none survived in SW. Hatching success of eggs (30 eggs each) was significantly higher in FW (mean: 73%) and 1/3 SW (73%) than in SW (19%). Tolerance of newly hatched larvae to salinity and temperature was investigated in different combinations of salinities (FW, 1/3 SW and SW) and temperatures (18, 23 and 28 °C). Larval survival was significantly different in each salinity and temperature. Survival rate was significantly higher in 1/3 SW than in FW and higher in SW than in FW at 23 °C and 28 °C. At the latter part of the experiment, there was no survival in FW and at 28 °C. Survival was higher in lower temperatures, but larval development did not occur in FW. Specific gravity of newly hatched larvae was 1.036 at 28 °C and 1.034 at 23 °C. When exposed to a light source on one side of an aquarium, larval distribution was not affected. Our results indicated larval S. japonicus are more adapted to brackish water and seawater than freshwater, while the adults and eggs are more adapted to freshwater and brackish water than seawater. This is consistent with their amphidromous life history with growth and spawning occurring in freshwater and the larval stage utilizing marine habitats.     

Rapid evolutionary loss of metal resistance revealed by hatching decades‐old eggs

We investigated the evolutionary response of an ecologically important freshwater crustacean, Daphnia, to a rapidly changing toxin environment. From the 1920s until the 1960s, the use of leaded gasoline caused the aquatic concentration of Pb to increase at least fivefold, presumably exerting rapid selective pressure on organisms for resistance. We predicted that Daphnia from this time of intense pollution would display greater resistance than those hatched from times of lower pollution. This question was addressed directly using the resurrection ecology approach, whereby dormant propagules from focal time periods were hatched and compared. We hatched several Daphnia genotypes from each of two Swiss lakes, during times of higher (1960s /1980s) and lower (2000s) lead stress, and compared their life histories under different laboratory levels of this stressor. Modern Daphnia had significantly reduced fitness, measured as the population growth rate (λ), when exposed to lead, whereas those genotypes hatched from times of high lead pollution did not display this reduction. These phenotypic differences contrast with only slight differences measured at neutral loci. We infer that Daphnia in these lakes were able to rapidly adapt to increasing lead concentrations, and just as rapidly lost this adaptation when the stressor was removed.     

Adaptive difference in daily timing of hatch in two locust species,Schistocerca gregaria and Locusta migratoria: The effects of thermocycles and phase polyphenism

This study examined the effects of temperature and phase polyphenism on egg hatching time in the desert locust, Schistocerca gregaria, and the migratory locust, Locusta migratoria. The two species exhibited differences and similarities in hatching behavior when exposed to different temperature conditions. In 12-h thermocycles of various temperatures, the S. gregaria eggs hatched during the cryoperiod (low temperature period), whereas L. migratoria eggs hatched during the thermoperiod (high temperature period). The eggs of both species hatched during the species-specific period of the thermoperiod in response to a temperature difference as small as 1 °C. Furthermore, the locusts adjusted hatching time to a new thermal environment that occurred shortly before the expected hatching time. In both species, the hatching of the eggs was synchronized to a specific time of the day, and two hatching peaks separated by approximately 1 day were observed at a constant temperature after the eggs were transferred from thermocycles 3 days before hatching. Eggs laid by gregarious females hatched earlier than those laid by solitarious females in S. gregaria but this difference was not observed in L. migratoria.     

Laying‐sequence variation in yolk carotenoids and egg characteristics in the red‐winged blackbird Agelaius phoeniceus

In many bird species with asynchronous hatching, smaller, later‐hatched nestlings are out‐competed for food by their larger, earlier‐hatched siblings and therefore suffer increased mortality via starvation. It is thought that female birds can either maintain or reduce the survival disadvantage of later‐hatched nestlings by differentially allocating maternal resources across the eggs of a clutch. Carotenoid pigments are an example of resources that female birds allocate differentially when producing a clutch, but laying sequence patterns for these pigments remain poorly studied in North American songbirds. We examined intraclutch variation in yolk carotenoids and egg metrics in 27 full clutches of red‐winged blackbird Agelaius phoeniceus eggs collected from eight wetlands in central Alberta, Canada. We predicted that carotenoids would decrease across the laying sequence, as in this species, later‐hatched, marginal nestlings suffer greater mortality than earlier‐hatched, core nestlings. We found nine carotenoid pigments in red‐winged blackbird egg yolks, including two that have never been described from avian yolks: α‐doradexanthin and adonirubin. As predicted, concentrations and amounts of most carotenoids decreased across the laying sequence, suggesting that female red‐winged blackbirds depleted their carotenoid resources as they laid more eggs. However, egg mass and yolk mass both increased across the laying sequence, suggesting that female red‐winged blackbirds may use other maternal resources to compensate for the size and survival disadvantage experienced by later‐hatched, marginal nestlings.     

Changes in morphology and cell number of inner cell mass of porcine blastocysts during freezing

Changes in the morphology and cell number of the inner cell mass (ICM) of porcine blastocysts at the expanded and hatched stages during freezing (-6.8 degrees C, -35 degrees C and -196 degrees C) were studied by differential fluorochrome staining. The shape of each ICM cell from fresh blastocysts at the expanded and hatched stages was sharply delineated but that of ICM cells from frozen blastocysts was partially distorted. The cell-to-cell contact of the ICM from fresh blastocysts was tight, while that from frozen blastocysts was loose or scattered. The percentages (18 to 38%) of expanded and hatched blastocysts with tight-contact ICM cells from frozen groups at each step were significantly lower (P<0.05) than that (100%) from fresh blastocysts. The number of live ICM cells and their proportion from frozen expanded blastocysts (10.9, 12,4% at -36 degrees C) were significantly lower (P<0.05) than those from fresh embryos (18.4, 19.1%) and at -196 degrees C (20.6, 18.4%). At the hatched stage, the number of live ICM cells and their proportion were not significantly different between each freezing step. These results show that the ICM of porcine embryos at both the expanded- and hatched-blastocysts stages survived even after freezing at -196 degrees C and that the degree of ICM damage was lower at the hatched stage than at the expanded stage.     

Ecological mismatches are moderated by local conditions for two populations of a long‐distance migratory bird

Ecological mismatches between reproductive events and seasonal resource peaks are frequently proposed to be a key driver of population dynamics resulting from global climate change. Many local populations are experiencing reduced reproductive success as a consequence of mismatches, but few mismatches have led to species‐level population declines. To better understand this apparent paradox, we investigated the breeding phenology and chick survival of two disjunct populations of Hudsonian godwits Limosa haemastica breeding at Churchill, Manitoba and Beluga River, Alaska. Only one population experienced a mismatch: godwits bred nearly one week after the onset of the invertebrate peak at Churchill because of asynchronous climatic change occurring throughout their annual cycle. However, chicks were not uniformly affected by the mismatch — growth rates and survival of young chicks were not correlated with invertebrate abundance, but older chicks tended to suffer lower survival rates on days of low invertebrate abundance. Ecological mismatches thus resulted in a complex array of consequences, but nonetheless contributed to reductions in chick survival. In contrast, godwits at Beluga River hatched their chicks just before the invertebrate peak, such that the period of highest energetic need coincided with the period of highest invertebrate abundance. As a result, growth rates and survival of godwit chicks were unaffected by invertebrate abundance. Godwits at Beluga River were able to properly time their reproduction because of predictable rates of climatic change and strong selection imposed by high predation on late‐hatched chicks. Taken together, our results suggest that population‐specific, local‐scale selection pressures play a critical role in determining the degree and severity of ecological mismatches. The potential for global climate change to induce species‐level population declines may therefore be mediated by the spatial variation in the selection pressures acting across a species’ range.     

Considerations in video playback design: using optic flow analysis to examine motion characteristics of live and computer-generated animation sequences

The increasing use of the video playback technique in behavioural ecology reveals a growing need to ensure better control of the visual stimuli that focal animals experience. Technological advances now allow researchers to develop computer-generated animations instead of using video sequences of live-acting demonstrators. However, care must be taken to match the motion characteristics (speed and velocity) of the animation to the original video source. Here, we presented a tool based on the use of an optic flow analysis program to measure the resemblance of motion characteristics of computer-generated animations compared to videos of live-acting animals. We examined three distinct displays (tail-flick (TF), push-up body rock (PUBR), and slow arm wave (SAW)) exhibited by animations of Jacky dragons (Amphibolurus muricatus) that were compared to the original video sequences of live lizards. We found no significant differences between the motion characteristics of videos and animations across all three displays. Our results showed that our animations are similar the speed and velocity features of each display. Researchers need to ensure that similar motion characteristics in animation and video stimuli are represented, and this feature is a critical component in the future success of the video playback technique.