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Chapter 14 : Long-Distance Dispersal of Fungi

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Abstract:

The relative degree to which organisms move is a process operating at multiple temporal and physical scales ( ). In recent years dispersal has received a great deal of attention in fields ranging from mathematics and physics to ecology and molecular biology, but only a patchy framework exists to explain dispersal over very large distances. Modeling patterns of long-distance dispersal (LDD) among macroorganisms, ranging from vertebrates and flying insects to seed plants, appears tractable, but documenting the geographic distributions and dispersal dynamics of microscopic propagules and microbes presents multiple theoretical and methodological challenges ( ). The majority of empirical research directly measuring the dispersal of microbes or microscopic propagules is restricted to relatively short distances, and tracking dispersal at greater spatial scales involves mathematical or genetic models, e.g., in studies of moss ( ), ferns ( ), bacteria ( ), and fungi ( ). However, fitting dispersal data (e.g., from the tracking of spore movement) to mathematical functions often over- or underestimates LDD and imprecisely describes the trajectory of spore movement across large distances ( ). Inferences based on population genetics data capture rare instances of successful LDD but incompletely describe underlying demographic processes and typically cannot speak to mechanisms of LDD ( ). Besides the limitations of mathematical and genetic methods, important details about the natural history of species are often ignored or remain unknown, leaving many questions unanswered, including, e.g., how ephemeral propagules remain viable while exposed to harsh environments over extended periods of time.

Citation: Golan J, Pringle A. 2017. Long-Distance Dispersal of Fungi, p 309-333. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0047-2016
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Figure 1

A framework for understanding fungal LDD.

Citation: Golan J, Pringle A. 2017. Long-Distance Dispersal of Fungi, p 309-333. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0047-2016
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Image of Figure 2
Figure 2

Sizes of fungal spores and other airborne particles. Some species are wind dispersed (e.g., ), while others have other means of dispersal (e.g., ). The smallest plant seed, , the pollen grains of and , and a glomerospore of the arbuscular mycorrhizal are provided for comparison. Species labeled with an asterisk are not fungi.

Citation: Golan J, Pringle A. 2017. Long-Distance Dispersal of Fungi, p 309-333. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0047-2016
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Figure 3

To integrate the disparate approaches used to describe and measure fungal LDD, we propose a synthetic three-part definition building on the general framework presented by Nathan ( ). A description of fungal LDD should include (i) identification of a source population and measure of source inoculum concentration (e.g., the number of spores in a single rust pustule), (ii) a measured and/or modeled dispersal kernel, and (iii) a measure of the distance, based on the dispersal kernel, past which only 1% of spores travel. Adopting a standard approach would mitigate the confusion caused by differing definitions and measurements of LDD and facilitate comparisons among the dispersal kernels of different species. In the illustration, the blue and red dispersal kernels demonstrate idealized kernels for two hypothetical species. LDD is defined per species at distances A and B, respectively—the distance beyond which only 1% of spores travel. We next used our approach with real dispersal data of (measured as the number of resistant lesions per square meter of banana leaf measured from a source to 1,000 m) ( ), (measured as the recovery rate of ascospores of a unique clone released from a source to 1,000 m) ( ), and (measured as the proportion of DNA from snow samples identical to an isolated source of soredia up to a distance of 40 m [ ]) to estimate dispersal kernels and identify LDD for each species. We smoothed the published data to estimate an approximate dispersal kernel, and the distance beyond which 1% of spores traveled was found by integrating the area under each kernel from 0 m to the distance at which 99% of spores had been captured. Although both and are capable of dispersing to approximately 1,000 m, the proportion of spores that fit our definition of LDD varies considerably, because LDD is defined past 714 m for and past 250 m for . A holistic comparison of the two dispersal kernels suggests that different dynamics will shape the effective reach of each species. The dispersal kernel of illustrates how truncated experimental setups can impact measures of LDD. At the furthest collection point (40 m), a large proportion of samples tested positive, and the best dispersal kernel that can be modeled from the data ( ) provides what is likely an underestimate of LDD, at approximately 39 m (15% of the positive samples collected at 0 m were detected). Ideally, the tail end of a modeled dispersal kernel should very closely approach a horizontal line at = 0.

Citation: Golan J, Pringle A. 2017. Long-Distance Dispersal of Fungi, p 309-333. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0047-2016
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Figure 4

A phylogram of genetic distances among 15 geographic populations of . The fact that geographically distant populations of are grouped together, e.g., Uruguayan populations are grouped with Algerian and Syrian populations, likely suggests movement mediated by humans. infects one of the most traded agricultural products (wheat), and its ascospores cannot survive prolonged exposure to, e.g., dry air ( ). Data adapted from Zhan et al. ( ); similar clustering of geographically distant populations is found from data on ( ), ( ), and ( ).

Citation: Golan J, Pringle A. 2017. Long-Distance Dispersal of Fungi, p 309-333. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0047-2016
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Figure 5

Images of various fungal spores. Basidiospores of (brown powder) next to seeds of (semicircles) and sugar crystals (white cubes). Urediniospores of (Fig. 1 of reference ). Conidia of and . is a putative long-distance disperser, while (10× in size) is not (courtesy of Steve Jordan). Glomerospore of (Fig. 5i of reference ). Conidium of (Fig. 5c of reference ). Teliospore of (Fig. 9 of reference ). Urediniospore of (Fig. 1e of reference ). Urediniospore size, shape, and ornamentation of (Fig. 1d of reference ). Zoospores of chytrid ( ). Ascospores of ( ). Sporangiospores of var. ( ). Basidiospores of still on soredia ( ). Conidia of the aquatic ascomycete (Fig. 66 of reference ).

Citation: Golan J, Pringle A. 2017. Long-Distance Dispersal of Fungi, p 309-333. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0047-2016
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Figure 6

Comparing spore sizes to reported maximum dispersal distances. Spore volume in square micrometers is measured on the left-hand vertical axis, and spore Q-ratio (the ratio of spore length to width) is measured on the right. Data points were calculated from the parameters listed in Table 1 . There is a poor correlation between approximate maximum dispersal distance and both average spore volumes (R = 0.0167, = 0.5568) and Q-ratios (R = 0.1113, = 0.1198). The lack of any correlation likely reflects inconsistent definitions and measurements of LDD, rather than any biological reality.

Citation: Golan J, Pringle A. 2017. Long-Distance Dispersal of Fungi, p 309-333. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0047-2016
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Figure 7

Images of spore dispersal structures among fungi. Basidiospores of carried vertically by evaporative airflows from mushroom cap (Fig. 1e of reference ). Hypogeous spore body of (Wikimedia Commons Creative Commons Attribution-Share Alike 3.0 Unported [WC]). Sporangium of releasing sporangiospores (courtesy of Andrii Gryganskyi). mushroom (Doug Collins, WC). Synchronous spore release from apothecia (Fig. 1b of reference ). Asci of ( ). Apothecia of ( ). Typical gilled agaric mushroom with gills to increase surface area of spore-producing tissue (WC).

Citation: Golan J, Pringle A. 2017. Long-Distance Dispersal of Fungi, p 309-333. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0047-2016
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Tables

Generic image for table
Table 1

Spore parameters for putative long-distance dispersers

Citation: Golan J, Pringle A. 2017. Long-Distance Dispersal of Fungi, p 309-333. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0047-2016