http://www.collembola.org/publicat/patholog.htm - Last updated on 2017.02.13 by Frans Janssens
Checklist of the Collembola: Note on pathogenic fungal infections in Symphypleona (Hexapoda: Collembola) from Europe

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

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.

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.

Fig.3. Dicyrtoma fusca from Holland
Dorso-lateral thoracic tumor
2012.11.18 © van Duinen, J.
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.
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).
Fig.1. Dicyrtoma fusca from Holland
Swollen trunk
2012.11.18 © van Duinen, J.
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.

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.
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).
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.
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

Fig.4a. Dicyrtoma fusca from Holland
Sporulation of Conidiobolus coronatus
2012.12.19 © van Duinen, J.
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?

Fig.aca. Predatory Acari from Holland
Sporulation
2012.07.15 © van Duinen, J.
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).
Fig.uk2. Dicyrtomina ornata from the UK
Infected by Neozygites sp.
2013.01.05 © Nurcombe, E.
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).
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.
Fig.uk3. Dicyrtomina saundersi from the UK
Infected by Conidiobolus coronatus
2013.12.28 © Phillips, E.
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.
Fig.holl3. Dicyrtomina saundersi from Holland
Infected by Conidiobolus coronatus
2014.02.06 © van Duinen, J.
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.
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.
Fig.uk5. Dicyrtomina saundersi ♂ from the UK
Infected by Conidiobolus coronatus
2017.02.07 © Horton, M.
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 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 Mick E. Talbot, Eddie Nurcombe, Andy Murray, Ed Phillips, Johan Myhrer, and Mark Horton for using their pictures as illustrations.

Bibliography