Landscape structure and ecology influence the spread of a bat fungal disease

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Landscape structure and ecology influence the spread of a bat fungal disease

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Landscape structure and ecology influence the spread of a bat fungal disease
Series Title:
Functional Ecology
Lilley, Thomas M.
Anttila, Jani
Ruokolainen, Lasse
Publication Date:


Subjects / Keywords:
Chiroptera ( local )
Dispersal ( local )
Landscape Structure ( local )
Opportunistic Pathogen ( local )
Outside‐Host Competition ( local )
White‐Nose Syndrome ( local )
Wns ( local )
serial ( sobekcm )


1. White‐nose syndrome (WNS), affecting multiple North American bat species during the hibernation period, is a highly pathogenic disease caused by the psychrophilic fungus Pseudogymnoascus destructans (Pd). Because the fungal pathogen persists in the hibernation site environment independently of the hosts, previous theory on spatial disease dynamics cannot predict WNS epidemics. However, the ability to understand factors contributing to the spread of white‐nose syndrome (WNS) in North America is crucial to the management of infected and susceptible bat populations as well as the conservation of threatened and endangered bat species. 2. Utilizing recent theory on environmental opportunistic pathogens, we modelled the effect of (a) landscape clustering, (b) environmental conditions in hibernacula and (c) microbial competition on the spread of WNS. We used available, already published data to construct and parameterize our model, which takes into account the spatial distribution of hibernation sites, temperature conditions in both the outside ambient and hibernation site environment, bat population dynamics, dispersal and infection by the pathogen, which also has its host‐independent dynamics with the environment. We also consider the effect of outside‐host competition between the pathogen and other micro‐organisms on spatial disease dynamics. 3. Our model suggests that pathogen loads accumulate in poorly connected hibernacula at short host dispersal, which can help found the epidemic. In contrast, invasion of the landscape is most successful at long host dispersal distances, with homogenous hibernation site distribution and heterogeneous between‐hibernation site temperatures. Also, increasing the mean temperature across hibernacula increases fungal growth rate, leading to higher disease prevalence and faster invasion rate. Increasing spatial heterogeneity in hibernaculum temperatures results in the formation of disease hotspots in warmer hibernacula, facilitating more effective spread of the d
Original Version:
Functional Ecology, Vol. 32, no. 11 (2018-06-25).

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K26-00079 ( USFLDC: LOCAL DOI )
k26.79 ( USFLDC: LOCAL Handle )

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Functional Ecology. 2018; 32 : 2483–2496. | 2483 | DOI: 10.1111/1365-2435.13183 RESEARCH ARTICLELandscape structure and ecology influence the spread of a bat fungal diseaseThomas M. Lilley1,2 |3 |3 Functional Ecology 1 2 3 Correspondence Funding information Pseudogymnoascus destructans Pd


| Fu nctional Ec olo g y | Pseudogymnoascus destructans Pd Pd Pseudogymnoascus and Pd


| Fu nctional Ec olo g y duced on Myotis lucifugus | | S E I Pd F M T Na Sa + Ea + Ia h T T Pd fun ID50 and ef P d Sh f


| Fu nctional Ec olo g y Parameter name Values r 1/day 0.0052 Kh b10 r b10 kr – 6 Kf 106f100 Km 106m100 e f 1/day 0.05 ID50 – 140 – 5 I 1/day 1/day d b 1/day 0.001 b0.2 c – 0.01 c3 – –1.0e4 c2 – 8.3e c1 – –8.3e c0 – 0.35 ah b8.0 kah – 10 ha b14.0 kha – 20 1/day 0.01 f 1/day 0.04 b 1/day 0.65 b; b – 1.25 b; b – bo bo b; b – 0.25 bo 15.0 bo 15.0; 14.0–16.0 cfm – 0.0; 0.5 cmf – 0.0; 0.0–1.0 cd 0.1 (Continues)


| Fu nctional Ec olo g y where no Pd Ia Ea I Ea Sa Pd T and Pd t t cd T = cT c Y c Y T T r T SD Parameter name Values c – 0.65 1.25; 0.5–2.0 – 102; 10103 To To 0.2; 0.0–0.4 Susceptible Exposed Infected Reproduction Fungal introduction + direct transmission Fungal clearance Disease loss Disease onset Spore transmission Spore shedding Death Death Deat h r(TA), Kh , ID 50, d, Ih, fhh E e Reproduction rf(TH), Kf Fungus Reproductionrm(TH), Km Interferencecfm, cmf Microbiota


| Fu nctional Ec olo g y Pd Pd cmf cfm F M rf T rm T F and M where T b1 b5 Pd b | were varied be 1 3 f x 2e xx x | Invasion rate invasion rate = tI n/ t tI and t n | T T rfntr


| Fu nctional Ec olo g y M. lucifugus T t t T 0 0.25 0.5 0.75 1Variability in mean temperature, (TH)0.0 0.1 0.2 0.3 0.4Dispersal scale ( )0.50 0.75 1.00 1.25 1.50 1.75 2.000 0.25 0.5 0.75 1Mean temperature in hibernacula, (T H ) Variability in mean temperature, (TH)7.0 7.2 7.4 7.6 7.8 8.00.0 0.1 0.2 0.3 0.4Landscape clustering (log 10 ( ))Dispersal scale ( )0.50 0.75 1.00 1.25 1.50 1.75 2.001.0 1.5 2.0 2.5 3.0 LOW HIGH LONG SHORT LONG SHORT(a) (b) (c) (d) Relative invasion time Relative invasion time local global


| Fu nctional Ec olo g y n = p < b = p < b = p = b T T T | of Pseudogymnoascus destructans M. lucifugus cfm T Tincreases T = 102 0.2 0.4 0.6 Risk of pathogen inf ection Top t10 0.51 2 0.0 0.2 0.4 0.00 0.25 0.50 0.75 1.00Competition pressure, c fm Pa thogen in va sion rate Top t10 0.51 2 0 250 500 750 10 0.51 2 T op t Mean time to in v asion Top t 1 0 0.5 1 2(a) (b) (c)


| Fu nctional Ec olo g y M. lucifugus Pd


| Fu nctional Ec olo g y Pd is Pd M. lucifugus Pd Pd M. lucifugus Pd by M. lucifugus ence of Pd Eptesicus fuscus M. lucifugus such as Perimyotis subflavus and Myotis septentrionalis M. lucifugus was by M. lucifugus of Pd . In areas where Pd hibernacula. Thomas M. Lilley Jani Anttila Lasse Ruokolainen Ecology 93


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| Fu nctional Ec olo g y Current Biology 23 Trends in Ecology & Evolution 12 Entomophaga maimaiga Lymantria dispar Environmental Entomology 19 Science Advances 2 Ecology Letters 18 PLOS Biology 7 Pseudogymnoascus destructans EcoHealth 12 s10393-014-0981-4 Proceedings of the Royal Society of London. Series B 283 Population ecology of the little brown bat, Myotis lucifugus, in Indiana and north-central Kentucky Functional and evolutionary ecology of bats mammals. Nature 418 Journal of Theoretical Biology 254 Journal of Theoretical Biology 275 PLoS ONE 6 Notes on foraging activity of female in Maryland. Res. Pap. NRS-8 Conservation and ecol ogy of Pennsylvania’s bats Science 294 Trends in Ecology & Evolution 25 Oecologia 183 Myotis sodalis Journal of Mammalogy 83 BioScience 58 Ecology Letters 15 Proceedings of the Royal Society BBiological Sciences 282 Philosophical transactions of the Royal Society of London. Series B, Biological Sciences 372 Open Science 3 Zenodo Pseudogymnoascus destructans Frontiers in Zoology 13 Myotis lucifugus Proceedings of the Royal Society of London. Series B 284 Geomyces destructans Nature 480 Geomyces de structans Applied and Environmental Microbiology 79


| Fu nctional Ec olo g y MSphere 1 Nature Communications 3 Pseudogymnoascus destructans Northeastern Naturalist 24 Journal of Applied Ecology 38 Proceedings. Biological Sciences 269 Ecosphere 2 Journal of Theoretical Biology 409 Pseudogymnoascus destructans PLoS ONE 12 Myotis lucifugus Journal of Mammalogy 94 Ecological Applications 25 Ecology and Evolution 2 Pseudogymnoascus destructans PLoS ONE 8 Journal of the Royal Society Interface 4 Proceedings of the Royal Society of London B: Biological Sciences 269 Journal of The Royal Society Interface 7 rsif.2009.0523 Pseudogymnoascus destructans Journal of Wildlife Diseases 51 Trends in Ecology & Evolution 24 Journal of Applied Ecology 51 Current Biology: CB 24 cub.2013.11.032 EcoHealth 4 Proceedings of the National Academy of Sciences of the United States of America 99 Proceedings of the Nutrition Society 58 Biological Conservation 160 Myotis lucifugus . Journal of Mammalogy 71 Ecology 36 White-nose syndrome: The devastat ing disease of hibernating bats in North America Ecology 85 Geomyces destructans PLoS ONE 7 BMC Physiology 14 Ecological Modelling 201 ecolmodel.2006.10.002 Geomyces destructans Proceedings of the National Academy of Sciences of the United States of America 109 The comparative ecophysiology of water balance in mi crochiropteran bats . In Symp Zool Soc Lond


| Fu nctional Ec olo g y Canadian Journal of Zoology 74 Biology Letters 7 Integrative and Comparative Biology 51 Pseudogymnoascus P. destructans PLoS ONE 12 Proceedings of the National Academy of Sciences of the United States of America 31 Trichoderma poly sporum Pseudogymnoascus destructans PLoS ONE 10 Pseudogymnoascus (Geomyces) de structans . PLoS ONE 9 Funct Ecol . 2018;32:2483–2496.


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