A model of insect—pathogen dynamics in which a pathogenic bacterium can also reproduce saprophytically

Godfray, H. C. J.; Briggs, Cheryl J.; Barlow, N. D.; O’Callaghan, Maureen; Glare, Travis R.; Jackson, Trevor A.

doi:10.1098/rspb.1999.0627

Cited by 32 publications

(33 citation statements)

References 32 publications

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“…The model allows free-living zoospores to reproduce saprobically, at a per capita rate determined by the parameter g. For analysis of the effect of a non-replicating resting stage, g is set to 0. The size of the free-living B. dendrobatidis population in the pond is limited by the function exp[K4Z(t)], which reduces saprobic reproduction as zoospore numbers increase, with 4 denoting the severity of density-dependent regulation (see Godfray et al (1999), who use this function to represent the population dynamics Figure 1. Schematic showing a model structure, including uninfected tadpoles, juveniles and adult B. bufo (P X , J X and A X , respectively), infected tadpoles (P Y ) and the free-living zoospore population (Z ).…”

Section: Methodsmentioning

confidence: 99%

“…Whether this is a resting stage or a saprobic form of the chytrid is still to be determined. Previous mathematical modelling has shown that pathogens with a saprobic free-living stage can drive their host population to extinction (Godfray et al 1999). Mathematical theory also suggests that pathogens with a long-lived resting stage can regulate their host population to very low levels, increasing the likelihood of stochastic population extinction (Anderson & May 1981).…”

Section: Introductionmentioning

confidence: 99%

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Persistence of the emerging pathogen Batrachochytrium dendrobatidis outside the amphibian host greatly increases the probability of host extinction

et al. 2007

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Pathogens do not normally drive their hosts to extinction; however, Batrachochytrium dendrobatidis, which causes amphibian chytridiomycosis, has been able to do so. Theory predicts that extinction can be caused by long-lived or saprobic free-living stages. The hypothesis that such a stage occurs in B. dendrobatidis is supported by the recent discovery of an apparently encysted form of the pathogen. To investigate the effect of a free-living stage of B. dendrobatidis on host population dynamics, a mathematical model was developed to describe the introduction of chytridiomycosis into a breeding population of Bufo bufo, parametrized from laboratory infection and transmission experiments. The model predicted that the longer that B. dendrobatidis was able to persist in water, either due to an increased zoospore lifespan or saprobic reproduction, the more likely it was that it could cause local B. bufo extinction (defined as decrease below a threshold level). Establishment of endemic B. dendrobatidis infection in B. bufo, with severe host population depression, was also possible, in agreement with field observations. Although this model is able to predict clear trends, more precise predictions will only be possible when the life history of B. dendrobatidis, including free-living stages of the life cycle, is better understood.

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Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Persistence of the emerging pathogen Batrachochytrium dendrobatidis outside the amphibian host greatly increases the probability of host extinction

et al. 2007

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Section: Retreat Sites Of Rain Forest Stream Frogs Are Not a Reservoimentioning

confidence: 99%

“…The broad host range of B. dendrobatidis also provides a reservoir of infection, enabling the species most susceptible to chytridiomycosis to be driven to extinction (Berger et al 2004). An alternative source of infection that could facilitate extinction is the persistence of free-living stages , Godfray et al 1999.A number of aquatic pathogens are able to persist as viable organisms in the environment by forming biofilms on both abiotic and biotic surfaces (Carli et al 1993, Hood & Winter 1997, Signoretto et al 2005. Zoospores of many chytrids can persist in films of water on plants and in soil, and in ponds and rivers (Carlile & Watkinson 1994), and have been detected on mossy rocks (Dewel et al 1985) and canopy leaves (Longcore 2005).…”

mentioning

confidence: 99%

Retreat sites of rain forest stream frogs are not a reservoir for Batrachochytrium dendrobatidis in northern Queensland, Australia

Rowley¹,

Skerratt²,

Alford³

et al. 2007

Dis. Aquat. Org.

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Chytridiomycosis is a potentially fatal disease of amphibians caused by Batrachochytrium dendrobatidis, and is implicated in declines and extinctions of amphibian populations and species around the world. To cause local host extinction, a disease organism must persist at low host densities. One mechanism that could facilitate this is the ability to persist in the environment. In the laboratory, B. dendrobatidis spreads by both frog-to-frog and environment-to-frog transmission, and can persist on a number of biotic substrates. In the field, B. dendrobatidis has been detected on environmental samples taken during an epidemic, but it is not known if it persists in the environment when endemic. Retreat sites of 2 species of Australian rain forest stream frogs Litoria lesueuri and L. nannotis were sampled 0 to 3 d after occupation during the wet and dry seasons in northern Queensland, Australia, where chytridiomycosis has been endemic for at least 10 yr. The intensity and prevalence of infection in frogs during sampling were comparatively low compared with epidemics. Diagnostic quantitative polymerase chain reaction did not detect B. dendrobatidis in any retreat site samples. It thus appears that retreat sites are not a major environmental source of infection when B. dendrobatidis occurs at low prevalence and intensity on frogs. This suggests that control efforts may not need to eliminate the organism from the environment, at least when prevalence and intensity of infection are low in frogs. Simply treating hosts may be effective at controlling the disease in the wild. KEY WORDS: Batrachochytrium dendrobatidis · Amphibian chytrid fungus · Chytridiomycosis · Environmental reservoir · Disease transmission · FrogsResale or republication not permitted without written consent of the publisher Dis Aquat Org 74: 7-12, 2007 B. dendrobatidis is the only chytrid known to cause disease in vertebrate hosts (Berger et al. 1998), presumably breaking down keratin that occurs in the epidermis of adult amphibians and the mouthparts of larval anurans. Chytridiomycosis can cause rapid mortality (Nichols et al. 2001), with infected frogs of susceptible species dying within 3 wk of infection in the laboratory (Berger et al. 1998(Berger et al. , 2004. In the laboratory, the disease is highly contagious (Nichols et al. 2001), spreading within and among individuals via motile, waterborne zoospores .One of the unusual aspects of chytridiomycosis is that it drives many host species to local extinction during outbreaks (Berger et al. 1998, Lips et al. 2006. For a pathogen to cause local host extinction it must be capable of persisting and infecting new hosts even at very low host population densities (Anderson & May 1986, Dobson & May 1986. One potential mechanism for this is the persistence and growth of Batrachochytrium dendrobatidis in tadpoles and adults that do not die from infection (Berger et al. 1998, 1999. The broad host range of B. dendrobatidis also provides a reservoir of infection, enabling the species most susceptib...

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“…Anderson & May 1981). The ability of generalist saprobes to become facultative pathogens has not been considered in as much detail, particularly in an ecological context (Godfray et al 1999).…”

Section: Introductionmentioning

confidence: 99%

Multihost saprobes are facultative pathogens of bullfrog Lithobates catesbeianus eggs

Ruthig¹,

Provost-Javier²

2012

Dis. Aquat. Org.

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Pathogens that infect more than one host species create complex linkages in ecological communities. We tested whether saprobes that grow on multiple host species in aquatic systems can be facultative pathogens of amphibian eggs. We isolated oomycetes from dead arthropods, vertebrates, plant leaves, and frog eggs that coexisted in a small pond. Analysis of internal transcribed spacer regions of rDNA (ITS1-5.8S-ITS2) indicated that several of the strains colonized more than one substrate, including bullfrog Lithobates catesbeianus eggs. In a controlled experiment, isolates from 7 different host species were pathogenic to L. catesbeianus eggs. These results demonstrate that dead organisms can serve as reservoirs for facultative pathogens.KEY WORDS: Oomycetes · Water molds · Multihost pathogen · Amphibian disease · Opportunistic pathogen · Internal transcribed spacer Resale or republication not permitted without written consent of the publisherDis Aquat Org 101: [13][14][15][16][17][18][19][20][21] 2012 Facultative pathogens that colonize more than one host species are particularly difficult for public health and wildlife officials to control. For example, the Australian fungal pathogen Cryptococcus gatti, which causes severe pulmonary and nervous system infections in humans and other animals, has successfully spread through Canadian British Columbia by its ability to infect multiple host species and by being accidentally moved by humans (Kidd et al. 2004(Kidd et al. , 2007. Despite its pathogenic effects on animals, C. gatti most commonly colonizes trees and dead wood and can also persist on the soles of shoes and vehicle tires for months (Kidd et al. 2007).One group of organisms that has been well documented as both pathogens (Phillips et al. 2008) and saprobes (Johnson et al. 2002) is water molds of the class Oomycota, family Saprolegniaceae. Species of oomycetes are pathogens of plants (Papavizas & Ayers 1964), algae (Gachon et al. 2009), vertebrates (Willoughby 1994 and invertebrates (Martin 1981, Oidtmann et al. 2004). Water molds have been found on eggs of amphibians around the world (e.g. Blaustein et al. 1994, Williamson & Bull 1994, Fernández-Benéitez et al. 2008, Ruthig 2008. However in some cases, water molds growing on amphibian eggs in the field were not pathogenic to eggs in controlled experiments. To date, eggs of green frogs Lithobates clamitans (Karraker & Ruthig 2009) and spotted salamanders Ambystoma maculatum , Karraker & Ruthig 2009) have been found to be resistant to infection when exposed to oomycete strains that were isolated from egg masses in the field. In cases where water molds did not infect their hosts in experiments, the oomycetes have been proposed to be acting saprobically in the field (Karraker & Ruthig 2009).Recent advances in molecular identification of water molds using the internal transcribed spacer (ITS) region (White et al. 1990) have uncovered a diversity of water molds within aquatic communities (Petrisko et al. 2008). Within a pond, different amphibian spe...

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A model of insect—pathogen dynamics in which a pathogenic bacterium can also reproduce saprophytically

Cited by 32 publications

References 32 publications

Persistence of the emerging pathogen Batrachochytrium dendrobatidis outside the amphibian host greatly increases the probability of host extinction

Persistence of the emerging pathogen Batrachochytrium dendrobatidis outside the amphibian host greatly increases the probability of host extinction

Retreat sites of rain forest stream frogs are not a reservoir for Batrachochytrium dendrobatidis in northern Queensland, Australia

Multihost saprobes are facultative pathogens of bullfrog Lithobates catesbeianus eggs

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