Dispersal may limit the occurrence of specialist wood decay fungi already at small spatial scales

We used species‐specific spore traps to measure airborne dispersal of the wood decay fungus Phlebia centrifuga (spore size 6.5–9 × 2.5–3 μm) up to 1000 m distance from a point source. We fitted two simple dispersal models, an empirical power law model and a semi‐mechanistic diffusion model to the data using the Bayesian approach. The diffusion model provided a better fit than the power law model which underestimated deposition at 3–55 m and overestimated deposition at longer and shorter distances. Model fit improved by allowing overdispersion, suggesting that spores are not dispersed independently but wind can transport spores in groups inside discrete air packages up to considerable distances. Using the fitted diffusion model and available information on the establishment rates of wood‐decay fungi, we examine the distance up to which colonisation from a single fruit body is likely to occur. We conclude that the diluting effect of distance and low establishment success make the occurrence of P. centrifuga dispersal limited possibly already at the distance of tens of metres and very probably at a few hundred metres from the nearest fruit body, despite the fact that under favourable conditions a high proportion of the spores can disperse considerably further. This conclusion is likely to hold generally for those fungal species that inhabit fragmented landscapes, have specialised resource and habitat requirements, and have similar spore size and other dispersal traits as P. centrifuga.     

How far and how fast can mushroom spores fly? Physical limits on ballistospore size and discharge distance in the Basidiomycota

Active discharge of basidiospores in most species of Basidiomycota is powered by the rapid movement of a droplet of fluid, called Buller’s drop, over the spore surface. This paper is concerned with the operation of the launch mechanism in species with the largest and smallest ballistospores. Aleurodiscus gigasporus (Russulales) produces the largest basidiospores on record. The maximum dimensions of the spores, 34 × 28 μm, correspond to a volume of 14 pL and to an estimated mass of 17 ng. The smallest recorded basidiospores are produced by Hyphodontia latitans (Hymenochaetales). Minimum spore dimensions in this species, 3.5 × 0.5 μm, correspond to a volume of 0.5 fL and mass of 0.6 pg. Neither species has been studied using high-speed video microscopy, but this technique was used to examine ballistospore discharge in species with spores of similar sizes (slightly smaller than A. gigasporus and slightly larger than those of H. latitans). Extrapolation of velocity measurements from these fungi provided estimates of discharge distances ranging from a maximum of almost 2 mm in A. gigasporus to a minimum of 4 μm in H. latitans. These are, respectively, the longest and shortest predicted discharge distances for ballistospores. Limitations to the distances traveled by basidiospores are discussed in relation to the mechanics of the discharge process and the types of fruit-bodies from which the spores are released.     

Ejection mechanics and trajectory of the ascospores of Gibberella zeae (anamorph Fuarium graminearum)

Since wind speed drops to zero at a surface, forced ejection should facilitate spore dispersal. But for tiny spores, with low mass relative to surface area, high ejection speed yields only a short range trajectory, so pernicious is their drag. Thus, achieving high speeds requires prodigious accelerations. In the ascomycete Gibberella zeae, we determined the launch speed and kinetic energy of ascospores shot from perithecia, and the source and magnitude of the pressure driving the launch. We asked whether the pressure inside the ascus suffices to account for launch speed and energy. Launch speed was 34.5 ms-1, requiring a pressure of 1.54 MPa and an acceleration of 870,000 g--the highest acceleration reported in a biological system. This analysis allows us to discount the major sugar component of the epiplasmic fluid, mannitol, as having a key role in driving discharge, and supports the role of potassium ion flux in the mechanism.     

Adaptation of the Spore Discharge Mechanism in the Basidiomycota

Background

Spore discharge in the majority of the 30,000 described species of Basidiomycota is powered by the rapid motion of a fluid droplet, called Buller''s drop, over the spore surface. In basidiomycete yeasts, and phytopathogenic rusts and smuts, spores are discharged directly into the airflow around the fungal colony. Maximum discharge distances of 1–2 mm have been reported for these fungi. In mushroom-forming species, however, spores are propelled over much shorter ranges. In gilled mushrooms, for example, discharge distances of <0.1 mm ensure that spores do not collide with opposing gill surfaces. The way in which the range of the mechanism is controlled has not been studied previously.

Methodology/Principal Findings

In this study, we report high-speed video analysis of spore discharge in selected basidiomycetes ranging from yeasts to wood-decay fungi with poroid fruiting bodies. Analysis of these video data and mathematical modeling show that discharge distance is determined by both spore size and the size of the Buller''s drop. Furthermore, because the size of Buller''s drop is controlled by spore shape, these experiments suggest that seemingly minor changes in spore morphology exert major effects upon discharge distance.

Conclusions/Significance

This biomechanical analysis of spore discharge mechanisms in mushroom-forming fungi and their relatives is the first of its kind and provides a novel view of the incredible variety of spore morphology that has been catalogued by traditional taxonomists for more than 200 years. Rather than representing non-selected variations in micromorphology, the new experiments show that changes in spore architecture have adaptive significance because they control the distance that the spores are shot through air. For this reason, evolutionary modifications to fruiting body architecture, including changes in gill separation and tube diameter in mushrooms, must be tightly linked to alterations in spore morphology.     

Spore Dispersal and Plant Disease Gradients; a Comparison between two Empirical Models

Power law and exponential models were fitted to 325 sets of observations which described decreases with distance in deposition of air-borne or splash-borne spores, or pollen, or in amounts of plant disease caused by fungi, bacteria or viruses. There, was generally little difference between the models in the goodness of fit to these data, although deposition gradients for spores borne in splash droplets were fitted better by exponential models and gradients for fungi with air-borne spores less than 10 μm in diameter were fitted better by power law models. The exponential model has the property that the observed variable decreases by half as the distance from the source increases by a constant increment (the half-distance); this provides a measureof the gradient that is more easy to visualize than the exponent in power law model. The half-distances of gradients for air-borne pathogens were greater than those for splash-borne or soil-borne pathogens. The exponential model is easier to incorporate into models of disease development than the power law model because the boundary condition at the source (the estimated number of spores or amount of disease at the source) is finite rather than infinite. However, both these empirical models have limitations and should not be extrapolated to distances outside the observed range.     

Modeling mycorrhizal fungi dispersal by the mycophagous swamp wallaby (Wallabia bicolor)

Despite the importance of mammal‐fungal interactions, tools to estimate the mammal‐assisted dispersal distances of fungi are lacking. Many mammals actively consume fungal fruiting bodies, the spores of which remain viable after passage through their digestive tract. Many of these fungi form symbiotic relationships with trees and provide an array of other key ecosystem functions. We present a flexible, general model to predict the distance a mycophagous mammal would disperse fungal spores. We modeled the probability of spore dispersal by combining animal movement data from GPS telemetry with data on spore gut‐retention time. We test this model using an exemplar generalist mycophagist, the swamp wallaby (Wallabia bicolor). We show that swamp wallabies disperse fungal spores hundreds of meters—and occasionally up to 1,265 m—from the point of consumption, distances that are ecologically significant for many mycorrhizal fungi. In addition to highlighting the ecological importance of swamp wallabies as dispersers of mycorrhizal fungi in eastern Australia, our simple modeling approach provides a novel and effective way of empirically describing spore dispersal by a mycophagous animal. This approach is applicable to the study of other animal‐fungi interactions in other ecosystems.     

Splash and grab: Biomechanics of peridiole ejection and function of the funicular cord in bird's nest fungi

The bird's nest fungi (Basidiomycota, Agaricales) package millions of spores into peridioles that are splashed from their basidiomata by the impact of raindrops. In this study we report new information on the discharge mechanism in Crucibulum and Cyathus species revealed with high-speed video. Peridioles were ejected at speeds of 1–5 m per second utilizing less than 2 % of the kinetic energy in falling raindrops. Raindrops that hit the rim of the basidiome were most effective at ejecting peridioles. The mean angle of ejection varied from 67 to 73° and the peridioles travelled over an estimated maximum horizontal distance of 1 m. Each peridiole carried a cord or funiculus that remained in a condensed form during flight. The cord unravelled when its adhesive surface stuck to a surrounding obstacle and acted as a brake that quickly reduced the velocity of the projectile. In nature, this elaborate mechanism tethers peridioles to vegetation in a perfect location for browsing by herbivores.     

Dispersal of Septoria nodorum Pycnidiospores by Simulated Raindrops in Still Air

Simulated raindrops, diameter c. 3 or 4 mm, fell 13 m down a raintower onto suspensions of Septoria nodorum pycnidiospores, depth 0.5 mm, or infected straw pieces. Splash droplets were collected on pieces of fixed photographic film. It was estimated that one drop generated c. 300 spore carrying splash droplets, containing c. 6000 spores, from a concentrated spore suspension (6.5 × 10⁵ spores/ml) and c. 25 spore-carrying droplets, containing c. 30 spores, from infected straw pieces (11 × 10⁶ spores/g dry wt). When the target was a spore suspension in water without surfactant, most spore-carrying droplets were in the 200—400 μm size category and most spores were carried in droplets with diameter >1000 μm. When surfactant was added to spore suspensions, most spore-carrying droplets were in the 0–200 μm category and most spores were carried in droplets with diameter 200–400 μm and none in droplets >1000 μm. Regression analyses showed a significant (p < 0.001) relationship between square root (number of spores per droplet) and droplet diameter; the slope of the regression line was greatest when surfactant was added to the spore suspensions. The distribution of splash droplets with distance travelled from the target was better fitted by an exponential model than by power law or Gaussian models. The distributions of spore-carrying droplets and spores with distance were fitted better by an exponential model than by a power law model. Thus regressions of log, (number collected) against distance were all significant (p < 0.01); the slopes of the regression lines were steepest when surfactant was added to the spore suspension. At a distance of 10 cm from target spore suspensions most splash droplets and spore-carrying droplets were collected at height 10–20 cm, with none above 40 cm; at a distance of 20 cm there were most at heights 0–10 cm and 40–50 cm.     

The drift distances and time spent in the drift by freshwater shrimps, Gammarus pulex, in a small stony stream, and their implications for the interpretation of downstream dispersal

1. The objectives were (i) to determine experimentally and to model the relationship between mean water velocity and both the mean distance travelled, and the mean time spent, in the drift by freshwater shrimps, Gammarus pulex; (ii) to develop a drift distance–water velocity model from the experimental study, and validate it with field data; (iii) to examine the relationship between drift rate, water velocity and benthic density with the latter expressed as a mean value for the whole stream and a mean value corrected for the distance travelled in the drift. 2. In field experiments at 10 water velocities (0.032–0.962 m s^?1), the significant relationship between the mean drift distance and mean water velocity was described both by a power function (power, 0.96) and a linear relationship. The mean drift time was fairly constant at 8.3 s (95% CL ± 0.4). A simple model estimated the drift distance and time spent in the drift by different percentages of the drifting invertebrates. This model predicted correctly the positive relationship between drift rate and water velocity for field data over a year. 3. The relationship between drift rate per hour and the independent variables, water velocity and benthic density, was well described by a multiple‐regression model. Adding temperature and date did not improve model fit. Variations in water velocity and benthic density explained 96% of the variation in nocturnal drift rate (65% to velocity, 31% to benthic density), but only 40% of the variation in diurnal drift rate (29% to velocity, 11% to benthic density). Correcting benthic density for the drift distances did not improve model fit. 4. The significance of this study is that it developed models to predict drift distances and time, values being similar to those obtained in another, larger stream. It also illustrated the importance of spatial scale in the interpretation of drift by showing that when drift distances were taken into account, the impact of drift on the population was higher (4–10% lost day^?1) than when drift distances were ignored (usually < 3% lost day^?1), especially at a local level.     

Sinking speeds of free-living phototrophic bacteria determined with covered and uncovered traps

Sinking of phototrophic bacteria in Lake Cis? was followed for2 years as a model for sinking of free-living bacterioplankton.A special trap system was deployed which included covered traps.This minimized problems created by turbulence in the water column.A correction for decomposition was also applied. Measured sinkingspeeds were then compared to expected sinking speeds accordingto Stokes' law. To calculate the latter, buoyant densities andvolumes of the cells were measured on several occasions andtheir values substituted into Stokes' equation. Bacteria didnot sink during periods of turbulence. During stratification,some periods of sinking could be detected. During such periods,bacteria sank with speeds in accordance with Stokes' law. Atother times, bacteria remained in suspension. Use of coveredtraps was shown to be necessary to correct overtrapping duringperiods of turbulence.     

Fungal Fragments as Indoor Air Biocontaminants

The aerosolization process of fungal propagules of three species (Aspergillus versicolor, Penicillium melinii, and Cladosporium cladosporioides) was studied by using a newly designed and constructed aerosolization chamber. We discovered that fungal fragments are aerosolized simultaneously with spores from contaminated agar and ceiling tile surfaces. Concentration measurements with an optical particle counter showed that the fragments are released in higher numbers (up to 320 times) than the spores. The release of fungal propagules varied depending on the fungal species, the air velocity above the contaminated surface, and the texture and vibration of the contaminated material. In contrast to spores, the release of fragments from smooth surfaces was not affected by air velocity, indicating a different release mechanism. Correlation analysis showed that the number of released fragments cannot be predicted on the basis of the number of spores. Enzyme-linked immunosorbent assays with monoclonal antibodies produced against Aspergillus and Penicillium fungal species showed that fragments and spores share common antigens, which not only confirmed the fungal origin of the fragments but also established their potential biological relevance. The considerable immunological reactivity, the high number, and the small particle size of the fungal fragments may contribute to human health effects that have been detected in buildings with mold problems but had no scientific explanation until now. This study suggests that future fungal spore investigations in buildings with mold problems should include the quantitation of fungal fragments.     

The metabolic cost of changing walking speeds is significant,implies lower optimal speeds for shorter distances,and increases daily energy estimates

Humans do not generally walk at constant speed, except perhaps on a treadmill. Normal walking involves starting, stopping and changing speeds, in addition to roughly steady locomotion. Here, we measure the metabolic energy cost of walking when changing speed. Subjects (healthy adults) walked with oscillating speeds on a constant-speed treadmill, alternating between walking slower and faster than the treadmill belt, moving back and forth in the laboratory frame. The metabolic rate for oscillating-speed walking was significantly higher than that for constant-speed walking (6–20% cost increase for ±0.13–0.27 m s⁻¹ speed fluctuations). The metabolic rate increase was correlated with two models: a model based on kinetic energy fluctuations and an inverted pendulum walking model, optimized for oscillating-speed constraints. The cost of changing speeds may have behavioural implications: we predicted that the energy-optimal walking speed is lower for shorter distances. We measured preferred human walking speeds for different walking distances and found people preferred lower walking speeds for shorter distances as predicted. Further, analysing published daily walking-bout distributions, we estimate that the cost of changing speeds is 4–8% of daily walking energy budget.     

Field experiments on seed dispersal by wind in ten umbelliferous species (Apiaceae)

This report presents data from experiments on seed dispersal by wind for ten species of the family Apiaceae. Seed shadows were obtained in the field under natural conditions, using wind speeds between four and ten m/s. The flight of individual seeds was followed by eye, and seed shadows were acquired, with median distances varying from 0.7 to 3.1 m between species. Multiple regression models of wind speed and seed weight on dispersal distance were significant for six out of ten species; wind speed had significant effects in seven cases, but seed weight only once. A good correlation between mean terminal falling velocity of the seeds of a species and median dispersal distance, indicates the promising explanatory power that individual terminal velocity data might have on dispersal distance, together with wind speed and turbulence. The theory that seeds that seem to be adapted to wind dispersal travel much longer distances than seeds that have no adaptation was tested. Flattened and winged seeds were indeed found to be transported further by wind, but not much further. Moreover, the species with wind-adapted seeds were also taller, being an alternative explanation since their seeds experienced higher wind speeds at these greater heights. Furthermore, flattened and winged seeds were disseminated from ripe umbels at lower wind speeds in the laboratory. This means that the observed difference in dispersal distance would have been smaller when species specific thresholds for wind speed were incorporated in the field experiments. We argue therefore, that seed morphology is not always the best predictor in classifying species in groups with distinctly different dispersal ability.     

Sporangium Exposure and Spore Release in the Peruvian Maidenhair Fern (Adiantum peruvianum,Pteridaceae)

We investigated the different processes involved in spore liberation in the polypod fern Adiantum peruvianum (Pteridaceae). Sporangia are being produced on the undersides of so-called false indusia, which are situated at the abaxial surface of the pinnule margins, and become exposed by a desiccation-induced movement of these pinnule flaps. The complex folding kinematics and functional morphology of false indusia are being described, and we discuss scenarios of movement initiation and passive hydraulic actuation of these structures. High-speed cinematography allowed for analyses of fast sporangium motion and for tracking ejected spores. Separation and liberation of spores from the sporangia are induced by relaxation of the annulus (the ‘throwing arm’ of the sporangium catapult) and conservation of momentum generated during this process, which leads to sporangium bouncing. The ultra-lightweight spores travel through air with a maximum velocity of ~5 m s^-1, and a launch acceleration of ~6300g is measured. In some cases, the whole sporangium, or parts of it, together with contained spores break away from the false indusium and are shed as a whole. Also, spores can stick together and form spore clumps. Both findings are discussed in the context of wind dispersal.     

Source strength of wheat pathogens during combine harvest

Many fungal pathogens of plants are dispersedaerially long distances and by this meansestablish disease foci and redistribute races.The goal of this research was to measure thesource strength of wheat pathogens duringharvest. Two fields in North Dakota wereplanted with spring wheat cultivar 2375 andcombined from windrows. A Rotorod model 20 airsampler attached to a helium balloon was liftedto 30 m and activated when the debris cloudfrom the combine passed the sampler location.The sampler was positioned 100 to 200 mdownwind from the field edge and 100 m upwindof the combine in field one. In this field,concentrations of Puccinia triticinauredospores were 1663 spores/m³ downwindand 19 spores/m³ upwind; also,Cochliobolus sativus conidia were 732spores/m³ downwind and 32 spores/m³upwind. In field two, downwind samples weretaken at heights of 6 m and 30 m on the fieldedge. In this field P. triticina sporeconcentration was 840 spores/m³ downwind.Also in field two, conidia of Pyrenophoratritici-repentis and teliospores ofUstilago sp. were each observed atconcentrations of 9 spores/m³. Many sporesappeared desiccated, but C. sativusspores germinated after 24 h in a moistchamber. Spore concentrations at the fieldmargin meant a minimal estimate of 10 billionspores were dispersed from the field per hourof combine operation; therefore, wheatharvesting liberates immense numbers of fungalpathogen spores, many of which then can bedispersed long distances in wind currents.     

Fungal fragments as indoor air biocontaminants

The aerosolization process of fungal propagules of three species (Aspergillus versicolor, Penicillium melinii, and Cladosporium cladosporioides) was studied by using a newly designed and constructed aerosolization chamber. We discovered that fungal fragments are aerosolized simultaneously with spores from contaminated agar and ceiling tile surfaces. Concentration measurements with an optical particle counter showed that the fragments are released in higher numbers (up to 320 times) than the spores. The release of fungal propagules varied depending on the fungal species, the air velocity above the contaminated surface, and the texture and vibration of the contaminated material. In contrast to spores, the release of fragments from smooth surfaces was not affected by air velocity, indicating a different release mechanism. Correlation analysis showed that the number of released fragments cannot be predicted on the basis of the number of spores. Enzyme-linked immunosorbent assays with monoclonal antibodies produced against Aspergillus and Penicillium fungal species showed that fragments and spores share common antigens, which not only confirmed the fungal origin of the fragments but also established their potential biological relevance. The considerable immunological reactivity, the high number, and the small particle size of the fungal fragments may contribute to human health effects that have been detected in buildings with mold problems but had no scientific explanation until now. This study suggests that future fungal spore investigations in buildings with mold problems should include the quantitation of fungal fragments.     

Natural folding of airborne fungal spores: a mechanism for dispersal and long-term survival?

Analysis of numerous air samples has indicated that dormant, viable fungal spores are highly present, which suggests that aerial dispersion is important for fungi. Whereas the majority of the spores may travel only very short distances, there is indication that a notable number of them cover much longer distances. Harmomegathy is a terminology coined by Wodehouse (1935) describing the natural folding of pollen to accommodate controlled and reversible water loss. Here, we discuss evidence that this concept may also apply to airborne fungal spores that face similar challenges and have to survive periods of drought and low temperatures while retaining viability to germinate after deposition upon a suitable moist substrate. In fact, (air)dried conidia, appear collapsed, survive for much longer times compared to spores in liquid, that deteriorate in time. This indicates that for some types of fungal spores, true dormancy is reached in the desiccated state. For these airborne spores this might be regarded as a pre-adaptation that supports long-distance transport of viable cells through air. We state that spores are naturally folded during transport in air if the humidity is low enough. We hypothesize that this is a pre-adaptation supporting release, dispersal and survival of airborne spores. Moreover, the smaller size of dry naturally-folded spores may also be relevant, e.g. for the opportunistic pathogenic fungus Aspergillus fumigatus reduced spore size supports deposition within the alveoli in the lung.     

Metabolic cost of motility in planktonic protists: Theoretical considerations on size scaling and swimming speed

The metabolic cost of swimming for planktonic protists is calculated, on theoretical grounds, from a simple model based upon Stokes' law. Energetic expenditure is scaled over both typically encountered size ranges (1–100 µm) and swimming speeds (100–5,000 µm/sec). In agreement with previous estimates for typical flagellates, these estimates generally suggest a low (<1%) cost for motility, related to total metabolic rate of growing cells. However, the cost of motility in small, fast-moving forms, such as some ciliates and flagellates, may be significant (1–10%) and even substantial (10–100%+) for certain species. In accordance with these predictions, many fast-moving ciliates restrict motility to bursts of activity or jumps. In the absence of a reduction in swimming speed or in the frequency of jumps, it is predicted that this relative cost of motility will be significantly increased in starving heterotrophs or light-limited autotrophs, if such cells reduce cell volumes and specific rates of respiration.     

Gliding locomotion of Siberian flying squirrels in low-canopy forests: the role of energy-inefficient short-distance glides

Short glides of less than 20 m seem energy inefficient for the Siberian flying squirrel Pteromys volans as with the northern flying squirrel Glaucomys sabrinus. However, Siberian flying squirrels in low-canopy forests frequently use short glides. Therefore, we sought to clarify the gliding patterns of Siberian flying squirrels for energy-efficient gliding transport in low-canopy forests (mean tree height, 15.3 m) in Hokkaido, Japan, based on records of 66 glides and 35 launch and landing trees. Mean launch height, landing height, and horizontal glide distance were 14.4, 2.7, and 21.4 m, respectively. For short distances, horizontal glide distance was strongly correlated with launch heights but not with launch tree height. For glides of more than 20 m, horizontal glide distance was significantly correlated with both launch height and launch tree height. The mean heights of launch and landing trees for short glides were 15.6 and 19.5 m, respectively. For long glides, these heights were 22.7 and 19.2 m. For short glides, mean launch tree height did not differ from overall mean tree height. However, for long glides, the mean launch tree height was greater than the overall mean tree height. Also, for short glides, the height of the landing tree was greater than that of the launch tree. Launch trees used for long glides were as high as the landing trees used in short glides. From these results, we conclude that Siberian flying squirrels in low-canopy forests save energy by gliding initially from a tree with sufficient height to permit a glide to a taller tree. This taller tree then permits long-distance glides that are energetically more efficient.     

Initial ball flight characteristics of curve and instep kicks in elite women's football

Initial ball flight characteristics of curve and instep kicks were investigated. Fifteen international female footballers performed curve and instep kicks from a distance of 20 m from goal and at a 1 m2 target. Seventeen Vicon cameras tracked three-dimensional coordinates of four reflective markers adhered to the ball. Ball flight characteristics were quantified, and the coordinates of the ball relative to the target center were recorded. The lateral launch angle and the angle of the spin axis relative to the horizontal best predicted the horizontal placement of the ball relative to the target. The vertical launch angle, antero-posterior velocity and amount of backspin best predicted the vertical coordinate. Regression models demonstrated how carefully controlled the flight characteristics must be with launch angles constrained within 3° to hit the target. Curve kicks were characterized by significantly greater lateral and vertical launch angles, increased sidespin and spin about the antero-posterior axis, and a more vertical spin axis. This information is beneficial for coaches in training players to achieve the characteristics required to score a goal and avoid a defensive wall. For example, if players consistently kick above or below the target, these findings identify the variables that will help rectify that error.