http://www.collembola.org/publicat/patholog.htm
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Last updated on
2019.02.25
by Frans Janssens
Frans Janssens,
Department of Biology, University of Antwerp, Antwerp, B-2020, Belgium
Jan J. van Duinen,
www.janvanduinen.nl, The Netherlands
Matty P. Berg,
Department of Ecological Science / Animal Ecology, VU University, AMsterdam, 1081HV, The Netherlands
Abstract
...
Methods and material
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Fig.0. Dicyrtoma fusca from Holland
Reference specimen
2012.11.22 © van Duinen, J.
On November 18, 2012, two specimens of
Dicyrtoma fusca (Lubbock, 1873)
were found
that were immobile and quite deformed,
therefore they appeared to be dead.
One was swollen severely (fig.1),
and the other had a large thoracic swelling (fig.3&4).
On November 20, 2012, another swollen specimen was found (fig.2).
On November 27, 2012, the first collapsed specimens were found (fig.col).
Subsequentially, additional specimens were recorded from the UK and from France.
All specimens were observed and photographed in situ.
Results
Primary observations
The first specimens were found in a recently reforesterisated part
of the nature reservate "De Zwatte",
near to Schoonloo, in Holland.
Never before such deformed specimens were observed in that regio.
Lots of other specimens of Dicyrtomina saundersi (Lubbock, 1862) and
Dicyrtoma fusca (Lubbock, 1873) (fig.0) with a normal habitus
were observed at that same location.
Two different types of pathology were observed:
1. thoracic tumor, and
2. severely swollen trunk.
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Fig.3. Dicyrtoma fusca from Holland
Dorso-lateral thoracic tumor
2012.11.18 © van Duinen, J.
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Fig.4. Dicyrtoma fusca from Holland
Dorso-lateral thoracic tumor
2012.11.18 © van Duinen, J.
Type 1: thoracic tumor.
The specimens from Holland show a spherical swelling dorso-laterally
at one of the thoracic segments.
Apparently, the cuticula is extremely elastic, locally,
given it did not burst due to the relatively large local swelling.
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Fig.ukmt. Dicyrtoma fusca from the UK
Swollen thorax
2013.02.18 © Talbot, M.E.
An additional observation of a specimen of Dicyrtoma fusca
with a swollen thorax,
from the UK, England, Lincolnshire, was recorded by Mick E. Talbot
on February 18, 2013 (fig.ukmt).
The swollen thorax appears to contain a more or less homogene substance
as that in the trunk of the specimen from Holland (see fig.1).
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Fig.frbn. Dicyrtoma fusca from France
Dorsal prothoracic tumor
2019.02.23 © Nogues, B.
Bernard Nogues recorded a specimen of Dicyrtoma fusca
with a swollen thorax from France, Essonne
on February 23, 2019 (fig.frbn).
The swelling on the thorax appears to be covered by conidia.
In addition there is a second swelling in the posterior part of the abdomen.
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Fig.1. Dicyrtoma fusca from Holland
Swollen trunk
2012.11.18 © van Duinen, J.
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Fig.2. Dicyrtoma fusca from Holland
Swollen trunk
2012.11.20 © van Duinen, J.
Type 2: swollen trunk.
In the affected specimens, the trunk (thorax + abdomen) is swollen in an
almost spherical fashion.
The small abdomen cannot be distinguished anymore.
The head remains normal.
The vesicles of the collophore are ejected (fig.2).
These are pressed against
the substrate in the watersurfacefilm as in the case of a dehydrated
specimen that wants to 'drink' by adsorbing water from the surfacefilm.
The specimens stand high on their legs (fig.1&2).
The furca is not extended backwards.
Both are indications that the specimens are not dead yet.
Possibly they are paralised, given they do hardly move.
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Fig.cut. Dicyrtoma fusca from Holland
Bursted epi/exocuticula
2012.11.26 © van Duinen, J.
The blown up trunk appears to contain a more or less homogene substance,
as if the body tissues are liquified.
The characteristic skin pigmentation cannot be recognised, suggesting the
epidermis has been liquified as well.
Note that the epi/exocuticula is bursted mediodorsally and longitudinally
from prothorax to small abdomen,
revealing the underlying endocuticula (fig.cut).
The endocuticula appears to be wet, an indication that it is hydrophile,
while the epi/exocuticula is water reppelent.
Also this suggest that the epidermis has been liquified,
given it is the epidermis
that produces the lipoproteins required to make the cuticula hydrophobe.
The endocuticula is more elastic than the epi/exocuticula and seems to serve
as a kind of stretchable membrane that holds the liquified body tissues.
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Fig.uk. Dicyrtoma fusca from the UK
Swollen trunk
2012.12.30 © Talbot, M.E.
An additional observation of a swollen specimen of Dicyrtoma fusca
from the UK, England, Lincolnshire, was recorded by Mick E. Talbot
on December 30, 2012 (fig.uk).
The swollen trunk appears to contain a more or less homogene substance
as in the specimen from Holland (see fig.1).
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Fig.sw. Dicyrtoma fusca from Holland
Swollen trunk
2013.01.05 © van Duinen, J.
More observations of swollen specimens of Dicyrtoma fusca
from Holland, Arnhem, Otterlo, were recorded
on January 5, 2013 (fig.sw).
Thus, the phenomenon is not restricted to the Schoonloo site.
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Fig.Sv. Sminthurus viridis from France
Swollen trunk
2017.12.07 © Tiky, S.
In addition, this observation of a swollen specimen of Sminthurus viridis
from France, was recorded
on December 07, 2017 (fig.Sv).
Thus, the phenomenon is neither restricted to Dicyrtominae nor to Holland.
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Fig.frbn2. Dicyrtoma fusca from France
Swollen abdomen
2019.02.24 © Nogues, B.
Bernard Nogues recorded a specimen of Dicyrtoma fusca
with a swollen abdomen from France, Essonne
on February 24, 2019 (fig.frbn2).
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Fig.col. Dicyrtoma fusca from Holland
Collapsed body
2012.11.27 © van Duinen, J.
Swollen bodies of specimens collaps eventually.
When a swollen specimen is touched, the body suddenly collapses (fig.col).
Secondary observations
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Fig.4a. Dicyrtoma fusca from Holland
Sporulation of Conidiobolus coronatus
2012.12.19 © van Duinen, J.
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Fig.4b. Dicyrtoma fusca from Holland
Conidia on unbranched conidiophores of Conidiobolus coronatus
2012.12.19 © van Duinen, J.
On December 19, 2012, specimens were observed that were covered with conidia
of Conidiobolus coronatus (fig. 4a)
on short unbranched conidiophores (fig. 4b).
Note the conidia are formed only on the old epi/exicuticula.
Note the highest density of conidia is at the thoracic tumor.
Question: is the infection of Conidiobolus coronatus a secondary
infection of the bursted specimen or is it the primary infection causing the
burst?
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Fig.aca. Predatory Acari from Holland
Sporulation
2012.07.15 © van Duinen, J.
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Fig.aca2. Acari:Parasitidae from Sweden
Sporulation
2015.07.dd © Myhrer, J.
Possibly, predatory mites may get infected as well when they have ingested
the body tissues of an infected prey (fig. aca, aca2).
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Fig.uk2. Dicyrtomina ornata from the UK
Infected by Neozygites sp.
2013.01.05 © Nurcombe, E.
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Fig.con. Dicyrtomina ornata from the UK
Infected by Neozygites sp.
Formation of conidia on unbranched conidiophores
2013.01.08 © Nurcombe, E.
A specimen of Dicyrtomina ornata
from the UK, England, Colwick Park, recorded by Eddie Nurcombe
on January 5, 2013 (fig.uk2)
showed many not yet sporulated conidiophores,
possibly of Neozygites sp.,
a genus of obligatory entomopathogenic fungi
typically found in Symphypleona (such as in Deuterosminthurus and Sphaeridia)
(Dromph & al. 2001:226),
growing out off the large abdomen.
On January 8, 2013, conidia were formed on unbranched conidiophores (fig.con).
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Fig.Sm. Sminthurides malmgreni ♂ from the UK
Swollen trunk
2013.02.03 © Murray, A.
An additional observation of an infected male specimen of Sminthurides malmgreni
from the UK, England, Dundon was recorded by Andy Murray
on February, 2013 (fig.Sm).
Note the severe swelling of the trunk.
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Fig.uk3. Dicyrtomina saundersi from the UK
Infected by Conidiobolus coronatus
2013.12.28 © Phillips, E.
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Fig.con3. Dicyrtomina saundersi from the UK
Infected by Conidiobolus coronatus
Formation of conidia on unbranched conidiophores
2013.12.28 © Phillips, E.
Dicyrtomina saundersi
from the UK, England, Moreton Morell, recorded by Ed Phillips
on December 28, 2013 (fig.uk3)
showed many not yet sporulated conidiophores
of Conidiobolus coronatus,
growing out off the large abdomen.
Some conidia on unbranched conidiophores were present on the thoracic
segments (fig.con3).
The latter suggests the fungal infection develops first in the thorax.
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Fig.holl3. Dicyrtomina saundersi from Holland
Infected by Conidiobolus coronatus
2014.02.06 © van Duinen, J.
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Fig.conholl3. Dicyrtomina saundersi from Holland
Infected by Conidiobolus coronatus
Begin of formation of unbranched conidiophores (*)
2014.02.06 © van Duinen, J.
Dicyrtomina saundersi
from Holland, recorded by Jan van Duinen
on Februari 2, 2014 (fig.holl3)
showed several conidiophores
of Conidiobolus coronatus,
beginning to grow out off the trunk (fig.hollcon3).
Note that only the trunk (thorax and abdomen) is affected.
It is completely covered in 'slime'.
The dorsal pigmentation patches of the skin have got a spotted appearance,
due to the digestive action of the mycelium of the fungus growing in it.
The epidermis, as well as the other internal organs, are digested completely,
eventually.
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Fig.uk4. Dicyrtomina sp. ♀ from the UK
Infected by Conidiobolus coronatus
2015.12.31 © Horton, M.
Dicyrtomina sp.
from the UK, England, Surrey, recorded by Mark Horton
on December 31, 2015 (fig.uk4)
showed many not yet sporulated conidiophores
of Conidiobolus coronatus,
growing out off the large abdomen.
In this specimen, the body is beginning to collaps.
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Fig.uk5. Dicyrtomina saundersi ♂ from the UK
Infected by Conidiobolus coronatus
2017.02.07 © Horton, M.
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Fig.conuk5. Dicyrtomina saundersi ♂ from the UK
Infected by Conidiobolus coronatus
Conidia almost sporulating.
2017.02.07 © Horton, M.
Dicyrtomina saundersi
from the UK, England, Surrey, Brookwood recorded by Mark Horton
on February 7, 2017 (fig.uk5)
showed many not yet sporulated conidiophores
of Conidiobolus coronatus,
growing out off the large abdomen.
Some conidia are almost sporulating (fig.conuk5).
Discussion
Apparently the specimens are infected by a lethal pathogenic fungus.
In case of such infections, often 'oedeem' is formed.
The infected specimen swells, and movement is slowed down up to death occurs.
The first well documented case of an entomophthoralean
fungus attacking Collembola is that of Neozygites sminthuri in
Sminthurus viridis from Denmark (Keller & Steenberg, 1997:21-24).
Entomophthorales are known for their host specificity
(Keller & Steenberg, 1997:24).
Fungal pathogens may be an important mortality factor of Collembola
(Dromph & al. 2001:231).
Sporulation of the pathogenic entomophthoralean fungus
Conidiobolus coronatus (Costantin) Batko
was observed in 10% of the specimens of a Dicyrtoma sp. population
from Denmark
(Dromph & al. 2001:227),
and the field prevalence peaked during August, reaching 17.8% infection.
(Dromph & al. 2001:230).
Conidia were formed on unbranched primary conidiophores.
All infected specimens collapsed soon after death and started to disintegrate.
No formation of rhizoids was observed.
(Dromph & al. 2001:228).
To be completed.
Conclusion
Specimens have been infected by a pathogen fungus, that
sporulates after a few days. The body of the infected host swells severely.
The swelling is limited to the trunk (thoracic and abdominal segments).
The head is never affected.
All Dicyrtominae specimens are recorded from the late autumn to winter period
(november to februari), the period in which many Dicyrtominae are
most active.
Acknowledgements
The authors wish to thank,
in chronological order,
Mick E. Talbot, Eddie Nurcombe, Andy Murray,
Ed Phillips, Johan Myhrer, Mark Horton, Sun Tiky and Bernard Nogues,
for using their pictures as illustrations.
Bibliography
