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A Third Way for Entomophthoralean Fungi to Survive the Winter: Slow Disease Transmission between Individuals of the Hibernating Host.

Eilenberg J, Thomsen L, Jensen AB - Insects (2013)

Bottom Line: Experimentally we documented that even at the low temperature of 5 °C, the fungus was able to maintain itself in Pollenia cohorts for up to 90 days.From these observations the full winter cycle of this fungus is elucidated.The three types of winter survival are discussed in relation to fungus epidemic development.

View Article: PubMed Central - PubMed

Affiliation: Department of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, DK 1871 Frederiksberg C., Denmark. Jei@life.ku.dk.

ABSTRACT
In temperate regions, insect pathogenic fungi face the challenge of surviving through the winter. Winter is a time when hosts are immobile, low in number or are present in a stage which is not susceptible to infection. Fungi from Entomophthoromycota have so far been known to survive the winter in two ways: either as (1) thick-walled resting spores released into environment from dead hosts, or as (2) structures inside the dead host (e.g., hyphal bodies). Here we report, from the Danish environment, a third way to survive the winter, namely a slow progression and transmission of Entomophthora schizophorae in adult dipteran Pollenia hosts that hibernate in clusters in unheated attics, sheltered areas outdoors (under bark etc.). Fungus-killed sporulating flies were observed outside very early and very late in the season. By sampling adults at the time of their emergence from hibernation in late winter/early spring we documented that the fungus was naturally prevalent and killed flies after a period of incubation. Experimentally we documented that even at the low temperature of 5 °C, the fungus was able to maintain itself in Pollenia cohorts for up to 90 days. From these observations the full winter cycle of this fungus is elucidated. The three types of winter survival are discussed in relation to fungus epidemic development.

No MeSH data available.


Related in: MedlinePlus

Three strategies for fungi from Entomophthoromycota to survive the winter in temperate climates. In all cases transmission of the fungus disease during spring, summer and autumn, is based on a rapid asexual cycle with conidia. (A) During winter, the fungus survives as thick walled resting spores, which after their release are found in the environment outside the host. After winter these resting spores germinate and produce infective conidia. (B) During winter the fungus survives outdoors as hyphal bodies inside either a dead host or a living, hibernating host. In the latter case the fungus is present as a latent infection. After winter these hyphal bodies produce infective conidia. (C) During winter the fungus survives in cool places indoors by a delayed transmission of conidial infections between individual hibernating hosts. After winter a proportion of these hibernating hosts infected during winter will die and produce infective conidia.
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insects-04-00392-f004: Three strategies for fungi from Entomophthoromycota to survive the winter in temperate climates. In all cases transmission of the fungus disease during spring, summer and autumn, is based on a rapid asexual cycle with conidia. (A) During winter, the fungus survives as thick walled resting spores, which after their release are found in the environment outside the host. After winter these resting spores germinate and produce infective conidia. (B) During winter the fungus survives outdoors as hyphal bodies inside either a dead host or a living, hibernating host. In the latter case the fungus is present as a latent infection. After winter these hyphal bodies produce infective conidia. (C) During winter the fungus survives in cool places indoors by a delayed transmission of conidial infections between individual hibernating hosts. After winter a proportion of these hibernating hosts infected during winter will die and produce infective conidia.

Mentions: We have illustrated three life history strategies of fungi from Entomophthoromycota in Figure 4. In all cases, the infection cycle during spring, summer and autumn is due to rapidly progressing infections by conidia. During winter, the dominant strategy for the fungus to survive outside the host is to overwinter as thick walled resting spores (Figure 4A). This is known for many host-pathogen systems involving fungi from Entomophthoromycota: such as Entomophaga maimaiga—Lymantria dispar [4,24], Entomophthora muscae—Delia radicum [1,25], Strongwellsea castrans—Delia radicum [1] and others [8]. A major advantage of this method of winter survival is that resting spores are resistant to abiotic factors such as subzero temperatures and drought; this resistance allows them to persist for months. There are two additional advantages to resting spores: First, they can sometimes be dispersed into soil where many host insects emerge as adults in the spring, and second, because they are the product of sexual reproduction, they maintain genetic variability. It is, however, questionable whether sexual reproduction takes place in all species [26]. A disadvantage is that resting spores may need a dormancy period [27] in order to germinate and to produce the infective units. Also, the presence of suitable hosts may trigger the germination of resting spores in spring [28]. A second method of winter survival is shown in Figure 4B. Here, the fungus is present in living or dead hosts as hyphal bodies or similar structures. When temperatures rise, these fungal structures can germinate and produce conidia. This winter survival strategy is known from E. planchoniana and its host Drepanosiphum acerinum, [6], where hyphal bodies were found in dead cadavers. It is also known from Neozygites floridana in the host Tetranychus urticae [7]. Here, the fungus survives outdoors in living, hibernating mite hosts, but the study did not include observations if transmission occurred between hosts during the winter. An advantage of this strategy is that once there is a temperature increase, hyphal bodies can quickly germinate and be transmitted to uninfected hosts. A disadvantage is that hyphal bodies are sensitive to external factors outdoors during a long winter.


A Third Way for Entomophthoralean Fungi to Survive the Winter: Slow Disease Transmission between Individuals of the Hibernating Host.

Eilenberg J, Thomsen L, Jensen AB - Insects (2013)

Three strategies for fungi from Entomophthoromycota to survive the winter in temperate climates. In all cases transmission of the fungus disease during spring, summer and autumn, is based on a rapid asexual cycle with conidia. (A) During winter, the fungus survives as thick walled resting spores, which after their release are found in the environment outside the host. After winter these resting spores germinate and produce infective conidia. (B) During winter the fungus survives outdoors as hyphal bodies inside either a dead host or a living, hibernating host. In the latter case the fungus is present as a latent infection. After winter these hyphal bodies produce infective conidia. (C) During winter the fungus survives in cool places indoors by a delayed transmission of conidial infections between individual hibernating hosts. After winter a proportion of these hibernating hosts infected during winter will die and produce infective conidia.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4553471&req=5

insects-04-00392-f004: Three strategies for fungi from Entomophthoromycota to survive the winter in temperate climates. In all cases transmission of the fungus disease during spring, summer and autumn, is based on a rapid asexual cycle with conidia. (A) During winter, the fungus survives as thick walled resting spores, which after their release are found in the environment outside the host. After winter these resting spores germinate and produce infective conidia. (B) During winter the fungus survives outdoors as hyphal bodies inside either a dead host or a living, hibernating host. In the latter case the fungus is present as a latent infection. After winter these hyphal bodies produce infective conidia. (C) During winter the fungus survives in cool places indoors by a delayed transmission of conidial infections between individual hibernating hosts. After winter a proportion of these hibernating hosts infected during winter will die and produce infective conidia.
Mentions: We have illustrated three life history strategies of fungi from Entomophthoromycota in Figure 4. In all cases, the infection cycle during spring, summer and autumn is due to rapidly progressing infections by conidia. During winter, the dominant strategy for the fungus to survive outside the host is to overwinter as thick walled resting spores (Figure 4A). This is known for many host-pathogen systems involving fungi from Entomophthoromycota: such as Entomophaga maimaiga—Lymantria dispar [4,24], Entomophthora muscae—Delia radicum [1,25], Strongwellsea castrans—Delia radicum [1] and others [8]. A major advantage of this method of winter survival is that resting spores are resistant to abiotic factors such as subzero temperatures and drought; this resistance allows them to persist for months. There are two additional advantages to resting spores: First, they can sometimes be dispersed into soil where many host insects emerge as adults in the spring, and second, because they are the product of sexual reproduction, they maintain genetic variability. It is, however, questionable whether sexual reproduction takes place in all species [26]. A disadvantage is that resting spores may need a dormancy period [27] in order to germinate and to produce the infective units. Also, the presence of suitable hosts may trigger the germination of resting spores in spring [28]. A second method of winter survival is shown in Figure 4B. Here, the fungus is present in living or dead hosts as hyphal bodies or similar structures. When temperatures rise, these fungal structures can germinate and produce conidia. This winter survival strategy is known from E. planchoniana and its host Drepanosiphum acerinum, [6], where hyphal bodies were found in dead cadavers. It is also known from Neozygites floridana in the host Tetranychus urticae [7]. Here, the fungus survives outdoors in living, hibernating mite hosts, but the study did not include observations if transmission occurred between hosts during the winter. An advantage of this strategy is that once there is a temperature increase, hyphal bodies can quickly germinate and be transmitted to uninfected hosts. A disadvantage is that hyphal bodies are sensitive to external factors outdoors during a long winter.

Bottom Line: Experimentally we documented that even at the low temperature of 5 °C, the fungus was able to maintain itself in Pollenia cohorts for up to 90 days.From these observations the full winter cycle of this fungus is elucidated.The three types of winter survival are discussed in relation to fungus epidemic development.

View Article: PubMed Central - PubMed

Affiliation: Department of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, DK 1871 Frederiksberg C., Denmark. Jei@life.ku.dk.

ABSTRACT
In temperate regions, insect pathogenic fungi face the challenge of surviving through the winter. Winter is a time when hosts are immobile, low in number or are present in a stage which is not susceptible to infection. Fungi from Entomophthoromycota have so far been known to survive the winter in two ways: either as (1) thick-walled resting spores released into environment from dead hosts, or as (2) structures inside the dead host (e.g., hyphal bodies). Here we report, from the Danish environment, a third way to survive the winter, namely a slow progression and transmission of Entomophthora schizophorae in adult dipteran Pollenia hosts that hibernate in clusters in unheated attics, sheltered areas outdoors (under bark etc.). Fungus-killed sporulating flies were observed outside very early and very late in the season. By sampling adults at the time of their emergence from hibernation in late winter/early spring we documented that the fungus was naturally prevalent and killed flies after a period of incubation. Experimentally we documented that even at the low temperature of 5 °C, the fungus was able to maintain itself in Pollenia cohorts for up to 90 days. From these observations the full winter cycle of this fungus is elucidated. The three types of winter survival are discussed in relation to fungus epidemic development.

No MeSH data available.


Related in: MedlinePlus