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Research Article
Checklist of thallus-forming Laboulbeniomycetes from Belgium and the Netherlands, including Hesperomyces halyziae and Laboulbenia quarantenae spp. nov.
expand article infoDanny Haelewaters§|, André De Kesel
‡ Purdue University, West Lafayette, United States of America
§ University of South Bohemia, Budějovice, Czech Republic
| Ghent University, Ghent, Belgium
¶ Meise Botanic Garden, Meise, Belgium
Open Access

Abstract

In this paper we present an updated checklist of thallus-forming Laboulbeniomycetes (Ascomycota, Pezizomycotina), that is, the orders Herpomycetales and Laboulbeniales, from Belgium and the Netherlands. Two species are newly described based on morphology, molecular data (ITS, LSU ribosomal DNA) and ecology (host association). These are Hesperomyces halyziae on Halyzia sedecimguttata (Coleoptera, Coccinellidae) from both countries and Laboulbenia quarantenae on Bembidion biguttatum (Coleoptera, Carabidae) from Belgium. In addition, nine new country records are presented. For Belgium: Laboulbenia aubryi on Amara aranea (Coleoptera, Carabidae) and Rhachomyces spinosus on Syntomus foveatus (Coleoptera, Carabidae). For the Netherlands: Chitonomyces melanurus on Laccophilus minutus (Coleoptera, Dytiscidae), Euphoriomyces agathidii on Agathidium laevigatum (Coleoptera, Leiodidae), Laboulbenia fasciculata on Omophron limbatum (Coleoptera, Carabidae), Laboulbenia metableti on Syntomus foveatus and S. truncatellus (Coleoptera, Carabidae), Laboulbenia pseudomasei on Pterostichus melanarius (Coleoptera, Carabidae), Rhachomyces canariensis on Trechus obtusus (Coleoptera, Carabidae), and Stigmatomyces hydrelliae on Hydrellia albilabris (Diptera, Ephydridae). Finally, an identification key to 140 species of thallus-forming Laboulbeniomycetes in Belgium and the Netherlands is provided. Based on the combined data, we are able to identify mutual gaps that need to be filled as well as weigh the impact of chosen strategies (fieldwork, museum collections) and techniques in these neighboring countries. The aim of this work is to serve as a reference for studying Laboulbeniomycetes fungi in Europe.

Keywords

2 new taxa, arthropod-associated fungi, Ascomycota, Herpomycetales, integrative taxonomy, key, Laboulbeniales

Introduction

Herpomycetales and Laboulbeniales are two orders within the class Laboulbeniomycetes (Ascomycota, Pezizomycotina), consisting of arthropod-associated biotrophs. Both orders are unique among related fungi in that they do not form hyphae; instead, thalli are produced by mitotic divisions from a two-celled ascospore. Herpomycetales was recently described and includes a single genus, Herpomyces Thaxt., with 27 described species–all associated with cockroaches (Blattodea) (Haelewaters et al. 2019b; Gutierrez et al. 2020). The Laboulbeniales order, on the other hand, successfully radiated on a wide range of hosts. Representatives of this order can be found in three arthropod subphyla, including mites and harvestmen (in subphylum Chelicerata), millipedes (in subphylum Myriapoda), and many orders of true insects (in subphylum Hexapoda). The vast majority of about 2,325 described species (Kirk 2019) are known from beetles (order Coleoptera), hence the common name once introduced for the group, “beetle hangers” (Cooke 1892). The early taxonomic history of these fungi is fraught with confusion (Blackwell et al. 2020), but the incorporation of sequence data has led to a conclusive placement of these fungi within Ascomycota (Blackwell 1994; Weir and Blackwell 2001; Schoch et al. 2009).

Early studies on Laboulbeniales (including Herpomyces at that time) in Belgium and the Netherlands are scarce. In Belgium, Collart (1945, 1947) and Rammeloo (1986) made noteworthy contributions, followed by multiple publications by De Kesel and colleagues (1989–present). The Laboulbeniomycetes from Belgium were for the first time summarized by De Kesel and Rammeloo (1992), who reported 1 species of Herpomyces and 47 species of Laboulbeniales. De Kesel et al. (2020) provided an updated – and illustrated – Catalogue of the Laboulbeniomycetes of Belgium, with a total of 115 species (3 Herpomycetales, 112 Laboulbeniales) from 222 host species. For more details regarding the study of Herpomycetales and Laboulbeniales in Belgium, we refer to De Kesel and Rammeloo (1992) and De Kesel et al. (2020). In the Netherlands, thus far, no effort has been made to publish a checklist.

The study of Laboulbeniales in the Netherlands started during a meeting of the Dutch Entomological Society in 1906, triggered by a question from Dr. Johannes P. Lotsy, then director of the “Rijksherbarium” (Leiden). In response, Prof. Dr. De Meijere remembered that he once observed an infected Drosophila funebris (Fabricius, 1787) fly, collected at the ARTIS Amsterdam Royal Zoo in 1904, but had not thought it worthy of mention at the time. Recent infected material of D. funebris from nature reserve De Kaaistoep has thus far always been associated with Stigmatomyces entomophilus (Peck) Thaxt. (Haelewaters et al. 2015b) and hence it is likely that S. entomophilus represents the very first report of Laboulbeniales from the Netherlands. The first published account was a developmental study of Stigmatomyces baeri H. Karst. by Boedijn (1923). The fungus was found on an atypical host – Fannia canicularis (Linnaeus, 1761); this fly is the only reported host for Fanniomyces ceratophorus (Whisler) T. Majewski, which is morphologically different from Boedijn’s (1923) drawings. We agree with Thaxter (1931) that the fungus was probably correctly identified by Boedijn, but perhaps the host was not.

Next, in the 1930s, only two species of Laboulbeniales were reported in the Netherlands: Laboulbenia cristata Thaxt. from Paederus riparius (Linnaeus, 1758) (Kossen 1936, 1938) and Laboulbenia flagellata Peyr. from Platynus spp. (Zaneveld 1938). It was not until Abraham Middelhoek (1906–1968) that the number of reported species of Laboulbeniales in the Netherlands would increase by 25 (Middelhoek 1941, 1942, 1943a, b, c, d, 1945, 1947a, b, 1949). Middelhoek was first an artist who, among other things, made stained glass windows. Only after World War II, he studied biology and raised an interest in fungi, particularly the Laboulbeniales. After Middelhoek, Laboulbeniales were forgotten about in the Netherlands except for a single paper by Meijer (1975), who proposed to use Laboulbeniales fungi as “biological tags” to trace migration patterns. Since 2012, Haelewaters and colleagues have published several papers dealing with Laboulbeniales in the Netherlands, which together have more than doubled the number of reported species in this country (De Kesel and Gerstmans 2012; Haelewaters 2012, 2013; Haelewaters et al. 2012a, b, 2014, 2015a, b, 2020; De Kesel et al. 2013; Haelewaters and De Kesel 2013; De Kesel and Haelewaters 2014, 2019; Haelewaters and van Wielink 2016). To date, 79 species of Laboulbeniales are reported from the Netherlands.

In this contribution we compile all available data from Belgium and the Netherlands. Keeping in mind that both countries show some geographical differences, especially due to specific soils and increasing altitude in the southern part of Belgium, we think a combined checklist makes sense at this point. This is mainly because the sampling effort for Laboulbeniomycetes in the southern part of Belgium has been much lower compared to the northern and central areas of the country (De Kesel et al. 2020). As a result, the bulk of Belgian and Dutch records come from biogeographically comparable regions. The here presented checklist is useful to illustrate where mutual gaps need to be filled and what the impact has been of the chosen strategies (fieldwork, museum collections) and trapping techniques. In combination with the recently published Belgian catalogue (De Kesel et al. 2020) presenting illustrations and identification keys to 115 taxa, this checklist will serve as a reference for mycologists, students, and scholars studying Laboulbeniomycetes fungi. In addition, this work is an appropriate starting point for an updated checklist of thallus-forming Laboulbeniomycetes from Europe–an ongoing project that needs to be updated, three decades after the massive undertaking of Santamaría et al. (1991).

Materials and methods

Specimen collection and morphological study

Insects were collected in Belgium and the Netherlands using pitfall traps and on an illuminated white screen at night. Specimens were preserved in 96–99% ethanol until they were screened for presence of thalli of Laboulbeniomycetes at 20–50× magnification. Thalli were removed from the host at the foot and mounted in Amann solution following the methods in De Kesel et al. (2020). Drawings and measurements were made using a BX51 light microscope (Olympus, Tokyo, Japan) with drawing tube, digital camera, and AnalySIS software (Soft Imaging System GmbH, Münster, Germany); or an an Olympus BH2 bright field compound microscope with SC30 camera and cellSens 1.18 imaging software.

Infected hosts found in Belgium and the Netherlands are preserved at Meise Botanic Garden (BR) and the Brabant Museum of Nature, Tilburg (NNKN), respectively. Microscope slides of Laboulbeniales are deposited at BR, FH, GENT, and NMBT (Thiers continuously updated).

DNA extraction, PCR amplification, sequencing

Three thalli of Laboulbenia quarantenae sp. nov. were used for DNA isolation using the REPLI-g Single Cell Kit (Qiagen, Stanford, California) with modifications (Haelewaters et al. 2019b). The DNA extract was stored at -20 °C until PCR amplification. Recent studies found that even though the internal transcribed spacer (ITS) region is a good marker for species delimitation in Laboulbeniomycetes, it is difficult to amplify in this group. Instead, the large subunit (LSU) of the ribosomal RNA gene has been put forward as a secondary barcode because it is easy to amplify and provides high discriminative resolution at species-level (e.g., Haelewaters et al. 2018; Sundberg et al. 2018b; Walker et al. 2018; Liu et al. 2020). The partial LSU was amplified using primers LIC15R (Miadlikowska et al. 2002) and LR6 (Vilgalys and Hester 1990). Sequencing was outsourced to Macrogen Europe (Amsterdam, the Netherlands) with the same PCR primers and an additional reverse primer, LR3 (Vilgalys and Hester 1990). Resulting forward and both reverse sequence reads were assembled and edited with Sequencher version 5.2.3 (Gene Codes Corporation, Ann Arbor, Michigan).

For Hesperomyces halyziae, molecular work had been done previously (Haelewaters et al. 2018). DNA was extracted using the Extract-N-Amp Plant PCR Kit (Sigma-Aldrich, St. Louis, Missouri) (methods in Haelewaters et al. 2015c). Seven thalli were placed in a 1.5 mL tube with 40 µL of Extraction Solution and sterilized sand. The tube was then placed in a FastPrep FP120 Cell Disrupter (Thermo Fisher Scientific, Waltham, Massachusetts) to mechanically crush fungal material at 5.5 m/s for 20 sec, and then on a heating block to incubate at 95 °C for 10 min. Finally, a total of 120 µL Dilution Solution was added to the mixture. Because we needed to define “H. virescens sensu stricto”, additional extractions from single Hesperomyces thalli removed from Chilocorus stigma (Say, 1835) were performed using the REPLI-g Single Cell Kit with modifications. Amplification of the ITS was done using primers ITS1f (Gardes and Bruns 1993) and ITS4 (White et al. 1990) as well as Hesperomyces-specific primers ITShespL and ITShespR (Haelewaters et al. 2019b). Purification and sequencing (same primers) of these PCR products were outsourced to Genewiz (Plainfield, New Jersey).

Phylogenetic analyses

Methods for both datasets – ITS for Hesperomyces, LSU for Laboulbenia – were largely identical. Sequences were downloaded from NCBI GenBank (https://www.ncbi.nlm.nih.gov/genbank/) and supplemented with sequences that were generated during this study. Sequences were aligned using MUSCLE version 3.7 (Edgar 2004), which is available on the CIPRES Science Gateway V. 3.3 (Miller et al. 2010). After alignment of the ITS dataset, partial SSU and partial LSU were removed by looking for the motifs 5’-ATCATTA-3’ (3’ end of SSU) and 5’-TGACCT-3’ (5’ start of LSU), and deleting downstream and upstream sequence data, respectively (Baral et al. 2018). For the LSU dataset, we unsuccessfully searched for the 5’-TGACCT-3’ motif. We then looked for the motif following 5’-TGACCT-3’ in a Hesperomyces sequence (GenBank acc. no. MG757513), which is 5’-CGGAT-3’, found this motif in the Laboulbenia dataset, and then realized that the 5’ start of LSU in Laboulbenia includes one nucleotide substitution compared to the conventional motif: 5’-TGGCCT-3’. We deleted the downstream sequence data to remove partial ITS. Next, ambiguously aligned regions and uninformative positions were removed using the command line version of trimAl v1.2 (Capella-Gutiérrez et al. 2009) with gap threshold = 0.6 and minimal coverage = 0.5. Models of nucleotide substitution were selected by considering the Akaike Information Criterion corrected for small samples (AICc) with ModelFinder Plus (Kalyaanamoorthy et al. 2017). Maximum likelihood (ML) was inferred for each dataset under the selected model with IQ-TREE (Nguyen et al. 2015; Chernomor et al. 2016). Ultrafast bootstrap (BS) analysis with 1000 replicates estimated branch support in the ML trees (Hoang et al. 2018).

Bayesian analyses were done using a Markov chain Monte Carlo (MCMC) coalescent approach implemented in BEAST 1.8.4 (Drummond et al. 2012), with a strict clock assuming a constant rate of evolution across the tree, a Yule Speciation tree prior (Yule 1925; Gernhard 2008), and the nucleotide substitution model as selected by jModelTest 2.1 (Darriba et al. 2012) under the AICc criterion. For each dataset, four runs were performed from a random starting tree for 10 million generations with a sampling frequency of 1000. All settings were entered in BEAUti 1.8.4 to generate an XML file, which was run in BEAST on the CIPRES Science Gateway (Miller et al. 2010). Resulting log files were entered in Tracer version 1.6 (Rambaut et al. 2014) to check MCMC trace plots for convergence and to assess effective sample sizes (ESS). A standard 10% burn-in was used resulting in overall ESS values of well above 200 for all sampled parameters. After removal of 10% burn-in, trees files were combined in LogCombiner 1.8.4. TreeAnnotator 1.8.4 was used to generate consensus trees with 0% burn-in and to infer the Maximum Clade Credibility tree with highest product of individual clade posterior probabilities (pp) for both datasets.

Trees with ML BS and Bayesian pp were visualized in FigTree version 1.4.3 (http://tree.bio.ed.ac.uk/software/figtree/) and edited in Adobe Illustrator 2020 version 24.1.1 (San Jose, California).

Checklist

For the checklist of thallus-forming Laboulbeniomycetes from Belgium and the Netherlands, we used De Kesel et al. (2020) for Belgium and all available published papers (since 1938 up to 2020) for the Netherlands. Laboulbeniomycetes and their hosts are listed alphabetically, starting with Herpomycetales, followed by Laboulbeniales. Fungal species are numbered throughout (1–140), authority and reference to the protologue are presented. For each fungus, hosts are presented alphabetically, with classification (order, family) and country in which the association has been reported: “Be” for Belgium, “Nl” for the Netherlands. No detailed collection information is shown except for new country records. In several instances, taxonomic notes are provided. Hosts are according to Vorst (2010) and Beccaloni et al. (2014). Names of fungi correspond to Index Fungorum (2020).

Identification key

The key to species of Laboulbeniomycetes in Belgium and the Netherlands is based on diagnostic characters referring to morphology and/or host taxa. It requires microscope equipment and morphological study as described in Benjamin (1971), Huldén (1983), Majewski (1994), Santamaría (1998), and De Kesel et al. (2020). Terminology follows Tavares (1985), Santamaría (1998, 2003), and De Kesel et al. (2020).

Results

The ITS dataset consisted of 31 Hesperomyces sequences (Table 1) and 724 characters, of which 462 were constant and 198 were parsimony-informative. The selected nucleotide substitution model under AICc was TVM+F+G4 (-lnL = 2790.545, ModelFinder Plus) and TVM+G (-lnL = 2786.8769, jModelTest 2). The Hesperomyces virescens sensu lato (Haelewaters et al. 2018) clade has maximum support from both ML and Bayesian analyses (Figure 1). Each of the nine clades within H. virescens s.l. consists of isolates from thalli removed from a single host species, except for the Adalia clade, which includes isolates from both A. bipunctata and A. decempunctata. One of the clades consists of isolates from Chilocorus stigma, the host on which H. virescens was originally described (Thaxter 1891). This clade, representative of Hesperomyces virescens sensu stricto, receives maximum support. The single isolate of Hesperomyces halyziae, from Halyzia sedecimguttata, is placed as sister to H. virescens s.l. from Harmonia axyridis (Pallas, 1773) (pp = 0.8).

Table 1.

Hesperomyces sequences used in phylogenetic analysis of the ITS dataset. Asterisks (*) indicate sequences that were generated during the course of this study.

Species Host Isolate GenBank (ITS) Reference
Hesperomyces coleomegillae Coleomegilla maculata 632A KF192888 Goldmann et al. (2013)
Coleomegilla maculate 635D KF192906 Goldmann et al. (2013)
Hesperomyces halyziae Halyzia sedecimguttata D. Haelew. 955b MG757813 Haelewaters et al. (2018)
Hesperomyces virescens s.s. Chilocorus stigma D. Haelew. 1444a MT373697* This paper
Chilocorus stigma D. Haelew. 1444b MT373698* This paper
Hesperomyces virescens s.l. Adalia bipunctata D. Haelew. 1193g MG757817 Haelewaters et al. (2018)
Adalia bipunctata D. Haelew. 1231a MG757821 Haelewaters et al. (2018)
Adalia bipunctata D. Haelew. 1232a MG757822 Haelewaters et al. (2018)
Adalia decempunctata D. Haelew. 1248b MG757823 Haelewaters et al. (2018)
Azya orbigera D. Haelew. 928g MG745343 Haelewaters et al. (2018)
Cheilomenes propinqua D. Haelew. 655c MG757804 Haelewaters et al. (2018)
Cheilomenes propinqua D. Haelew. 659b MG757805 Haelewaters et al. (2018)
Cheilomenes propinqua D. Haelew. 1259a MG757828 Haelewaters et al. (2018)
Cycloneda sanguinea D. Haelew. 924a MG757808 Haelewaters et al. (2018)
Cycloneda sanguinea D. Haelew. 1374a MG757831 Haelewaters et al. (2018)
Harmonia axyridis 352B KF192916 Goldmann et al. (2013)
Harmonia axyridis D. Haelew. 361a MG757801 Haelewaters et al. (2018)
Harmonia axyridis D. Haelew. 486c KT800044 Haelewaters et al. (2015c)
Harmonia axyridis D. Haelew. 669a MG757807 Haelewaters et al. (2018)
Harmonia axyridis D. Haelew. 1188g MG438317 Haelewaters et al. (2019b)
Harmonia axyridis D. Haelew. 1268d MG757830 Haelewaters et al. (2018)
Harmonia axyridis DH1 KF192920 Goldmann et al. (2013)
Harmonia axyridis LT1 KF192910 Goldmann et al. (2013)
Harmonia axyridis MT001 KT800048 Haelewaters et al. (2015c)
Olla v-nigrum D. Haelew. 954e MG757812 Haelewaters et al. (2018)
Olla v-nigrum D. Haelew. 1200h MG757819 Haelewaters et al. (2018)
Olla v-nigrum JP353b MG757799 Haelewaters et al. (2018)
Olla v-nigrum JP354b MG757800 Haelewaters et al. (2018)
Psyllobora vigintimaculata D. Haelew. 1250b MG757825 Haelewaters et al. (2018)
Psyllobora vigintimaculata D. Haelew. 1250c MG757826 Haelewaters et al. (2018)
Psyllobora vigintimaculata D. Haelew. 1251b MG757827 Haelewaters et al. (2018)
Figure 1. 

Maximum clade creditability tree of Hesperomyces isolates reconstructed from an ITS dataset, with H. coleomegillae as outgroup. The topology is the result of Bayesian inference performed with BEAST. For each node, ML BS (≥ 65) and Bayesian pp (≥ 0.7) are presented above/below the branch leading to that node. Hesperomyces virescens sensu lato is highlighted with light gray shading, isolates are color-coded by host; H. virescens sensu stricto and H. halyziae sp. nov. are highlighted with dark gray shading.

The LSU dataset consisted of 24 Laboulbenia sequences (Table 2) and 682 characters, of which 558 were constant and 63 were parsimony-informative. The selected nucleotide substitution model under AICc was TN+F+G4 (-lnL = 1876.681, ModelFinder Plus) and TrN+G (-lnL = 1872.4616, jModelTest 2). Our phylogenetic analyses show nine distinct species, which are all supported. The relationships among species are unresolved in different places, but this is not unsurprising because of extremely limited taxon sampling. Laboulbenia quarantenae holds an unresolved position in the tree but is clearly separated from both L. flagellata and the morphologically similar L. vulgaris, confirming its status as a separate species. Laboulbenia vulgaris isolates E10T2 and E11T6, which originated from Bembidion tetracolum, are placed among isolates of the same species removed from Ocys harpaloides. Interestingly, and in accordance with De Weggheleire (2019) and Haelewaters et al. (2019a), L. flagellata falls apart in three species. However, only ten isolates are included, originating from six host species, none of which were reported in the protologue (Peyritsch 1873). As a result, it is too early to make taxonomic decisions within this problematic taxon.

Table 2.

Laboulbenia sequences used in phylogenetic analysis of the LSU dataset. Asterisks (*) indicate sequences that were generated during the course of this study.

Species Host Isolate GenBank (LSU) Reference
Laboulbenia bruchii Neolema adunata D. Haelew. 1346b MN394843 Haelewaters et al. (2019a)
Laboulbenia collae Paranchus albipes D. Haelew. 1456a MN394844 Haelewaters et al. (2019a)
Paranchus albipes D. Haelew. 1456b MN394845 Haelewaters et al. (2019a)
Paranchus albipes D. Haelew. 1461b MN397131 Haelewaters et al. (2019a)
Laboulbenia quarantenae Bembidion biguttatum, ADK6448 E13T12 MT371368* This paper
Laboulbenia flagellata Agonum emarginatum, ADK6428 E13T1 MT703825* This paper
Agonum micans, ADK6332 D. Haelew. 1457a MN394851 Haelewaters et al. (2019a)
Agonum micans, ADK6332 D. Haelew. 1457b MN394852 Haelewaters et al. (2019a)
Agonum micans, ADK6332 D. Haelew. 1457c MN394853 Haelewaters et al. (2019a)
Agonum nigrum, ADK6445 E13T11 MT703826* This paper
Limodromus assimilis, ADK6329-1 D. Haelew. 1454a MN394849 Haelewaters et al. (2019a)
Limodromus assimilis, ADK6329-1 D. Haelew. 1454b MN394850 Haelewaters et al. (2019a)
Limodromus assimilis, ADK6329-2 D. Haelew. 1458a MN394854 Haelewaters et al. (2019a)
Loricera pilicornis H85-1 KY350538 Sundberg et al. (2018a)
Oxypselaphus obscurus, ADK6374 E11T11 MT703824* This paper
Laboulbenia pedicellata Dyschirius globosus H84-1 KY350537 Sundberg et al. (2018a)
Laboulbenia systenae Disonycha procera D. Haelew. 1342b MN394858 Haelewaters et al. (2019a)
Laboulbenia vulgaris Bembidion tetracolum, ADK6420 E10T2 MT703822* This paper
Bembidion tetracolum, ADK5557 E11E6 MT703823* This paper
Ocys harpaloides, ADK6330-1 D. Haelew. 1455a MN397135 Haelewaters et al. (2019a)
Ocys harpaloides, ADK6330-1 D. Haelew. 1455b MN397136 Haelewaters et al. (2019a)
Ocys harpaloides, ADK6330-2 D. Haelew. 1459a MN397137 Haelewaters et al. (2019a)
Ocys harpaloides, ADK6330-3 D. Haelew. 1460a MN397138 Haelewaters et al. (2019a)
Ocys harpaloides, ADK6353-1 E0T6 MT703821* This paper

Taxonomy

Hesperomyces halyziae Haelew. & De Kesel, sp. nov.

MycoBank No: 835489
Figure 3

Etymology

Referring to the host genus, Halyzia.

Diagnosis

Morphologically very similar to other taxa within H. virescens sensu lato, but forming a distinct species supported by ITS data. The ITS sequence shares 95.8–97.9% identity with H. virescens s.l. from Harmonia axyridis, and 96.5–95.4% with H. virescens s.l. from Adalia bipunctata/A. decempunctata. Unique molecular synapomorphies in the ITS at positions 478, 517, 652.

Types

Holotype : The Netherlands, Noord Brabant Province, Tilburg, nature reserve De Kaaistoep, 51.5333333N, 5.0166667E, 11 Aug. 2015, leg. H. Spijkers & P. van Wielink, on female Halyzia sedecimguttata (Linnaeus, 1758) (Coleoptera, Coccinellidae) (NNKN), slide D. Haelew. 955a (FH, 4 juvenile and 3 mature thalli, left elytron), reported as Hesperomyces virescens in Haelewaters and van Wielink (2016). Paratypes: Belgium, Province Vlaams-Brabant, Meise, Domein van Bouchout, 50.927925N, 4.333069E, 28 Mar. 2019, leg. C. Gerstmans, on H. sedecimguttata (BR, CG437–CG440), slides BR5020212155379V, BR5020212156406V, BR5020212157434V, and BR5020212158462V; reported as Hesperomyces virescens sensu lato in De Kesel et al. (2020). Ibid., 1 Apr. 2019, leg. C. Gerstmans, on H. sedecimguttata (BR, CG441–442), slides BR5020212159490V and BR5020212160236V; reported as Hesperomyces virescens sensu lato in De Kesel et al. (2020).

Description

Thallus 335–453 μm long from foot to perithecial apex; colored yellow except for a somewhat darker region right above the foot. Cell I obtriangular, 2.0–2.5× longer than broad, broadening distally, with very oblique septum I–II. Cell II longer than broad, 23–28 × 16–21 µm, subtrapezoidal in section. Cell III always smaller than cell II, 14–20 × 14–19 µm, with inflated dorsal cell wall. Primary appendage consisting of 4 superposed cells, 61–67 μm long; in the same axis as cells I and III, separated from the latter by the constricted primary septum; its basal cell somewhat longer than broad, longer than each of the remaining cells of the appendage; second to fourth cells carrying a single antherium externally, the fourth cell also carrying a second upwardly directed antherium. Antheridia flask-shaped, with slightly (dorsally and/or basally) curved efferent necks, the upper antheridium carrying at its dorsal side a pointed process, which represents the original ascospore apex. Cell VI with subparallel margins to broadening distally, 33–70 × 23–33 μm. Perithecium 194–291 × 62–86 μm (not including basal cells), symmetric or with the anterior margin convex and the posterior one almost straight or concave; broadest near the upper third, then gradually tapering towards the apex; apex complex with 2 short lower lobes, 2 upper (terminal) lobes, and 2 prominent lips surrounding the ostiole; lower lobes tapering to a rounded tip, the ventral lobe outwardly directed; terminal lobes unicellular, elongated, 29–42 μm in length, curved upwards and outwardly; ostiole with two lips, 25–29 μm in length, one lip triangular, the other slightly shorter, blunt or rounded, basally carrying the remainder of the trichogyne. Ascospores 70–85 μm long, with conspicuous slime sheath only surrounding the larger cell.

Material sequenced

The Netherlands, Noord Brabant Province, Tilburg, nature reserve De Kaaistoep, 51.5333333N, 5.0166667E, 11 Aug. 2015, leg. H. Spijkers & P. van Wielink, on female Halyzia sedecimguttata (Coleoptera, Coccinellidae) (NNKN), isolate D. Haelew. 955b (7 thalli, elytra, ITS: MG757813).

Hosts and distribution

On Halyzia sedecimguttata from Belgium and the Netherlands. Previously reported as H. virescens (Haelewaters and van Wielink 2016, Haelewaters et al. 2017) and H. virescens sensu lato (De Kesel et al. 2020). One unverified record is available from France (Justamond 2019).

Notes

Supported by multi-locus phylogenetic analyses and sequence-based species delimitation methods, Haelewaters et al. (2018) showed that H. virescens Thaxt. is a complex of multiple species, segregated by host. The authors proposed to “restrict H. virescens sensu stricto to those thalli found on Chilocorus stigma, the host species on which the fungus was originally described” (Thaxter 1891). Here, we included two isolates from C. stigma (Say, 1835), and found the clade representative of H. virescens sensu stricto. Based on this analysis and previous work (Haelewaters et al. 2018), we can start describing the individual clades as distinct species. A monographic work with formal descriptions for the seven other species within H. virescens s.l. is in preparation, but in the light of this checklist we decided to describe H. halyziae, which was only known from a single collection in the Netherlands until we recently collected it in Belgium (Mar.–Apr. 2019).

Haelewaters and van Wielink (2016) reported an infected specimen of Halyzia sedecimguttata from nature reserve De Kaaistoep in the Netherlands. In 1997–2015, 476 individuals of H. sedecimguttata were collected on a lighted white sheet and screened for presence of Laboulbeniales, only resulting in one individual (parasite prevalence 0.2%). In Belgium, a population of infected H. sedecimguttata was found at the Meise Botanic Garden. Specimens were collected in spring 2019 while they were leaving their overwintering place–deep cracks in the woodwork of a small forest chapel. Screening of 46 specimens of H. sedecimguttata revealed nine infected ones (parasite prevalence 19.5%). This ladybird species seems to overwinter singly or in small congregations in narrow overwintering places, including in leaf litter, under foliage on stone walls, on trunks and branches (Majerus and Williams 1989). This congregation behavior is beneficial for transmission of the fungus and is also observed in Harmonia axyridis (Haelewaters et al. 2017).

Morphologically, H. halyziae is very similar to what we have thus far accepted as H. virescens. Within the Kingdom Fungi, there is an incredible diversity that cannot be perceived through morphology. Cryptic species are being uncovered in Agaricomycetes (e.g., Stefani et al. 2014; Sánchez-García et al. 2016), Lecanoromycetes (e.g., Singh et al. 2015), Leotiomyces (e.g., Grünig et al. 2008), Pucciniomycetes (Bennett et al. 2011), Ustilaginomycetes (e.g., Li et al. 2017), and other major clades. And while the Laboulbeniales has been the subject of a large-scale study to estimate the global species richness of the group (Weir and Hammond 1997), cryptic diversity was not part of the equation. In other words, the number of estimated species of Laboulbeniales, between 15,000 and 75,000, is likely to be corrected to include cryptic species. We note that the recognition of H. halyziae is only possible through molecular data and host association. Our current understanding is that, within this species complex, there is a strict parasite-host association, with one parasite found only on one host. We think that this host specificity exists at the genus level, given the Adalia clade (Figure 1), which includes isolates from thalli removed from two host species within the same genus.

Laboulbenia quarantenae De Kesel & Haelew., sp. nov.

MycoBank No: 835490
Figure 4

Diagnosis

Morphologically similar to Laboulbenia vulgaris Peyr., but the insertion cell is attached to the lower fifth of the posterior margin of the perithecial wall and the outer appendage is composed of 4–6(–8) branches resulting from successive dichotomies starting at the suprabasal cell, which is poorly pigmented or nearly hyaline. The LSU sequence shares 89.7–98.0% identity with other sequenced taxa of Laboulbenia, 97.4% with L. flagellata from Agonum nigrum, 97.5–98.0% with L. flagellata from Limodromus assimilis, 97.0–98.0% with L. flagellata from Agonum emarginatum/A. micans/Loricera pilicornis/Oxypselaphus obscurus, and 97.0–97.7% with L. vulgaris from Bembidion tetracolum/Ocys harpaloides. Unique molecular synapomorphies in the LSU at positions 503, 545.

Types

Holotype : Belgium, Province Vlaams Brabant, Meise, Domein van Bouchout, 50.9267056N, 4.3220028E, 30 m a.s.l., 26 Apr. 2019, leg. A. De Kesel, rivulet-associated grassland, on Bembidion (Philochtus) biguttatum (Fabricius, 1779) (Coleoptera, Carabidae), ADK6448 (BR), slide BR5020212163329V (1 mature thallus, prothorax). Isotypes: ibid., slides BR5020212162292V (2 mature thalli, right mesofemur), BR5020212161264V (6 mature thalli, right protibia), BR5020212166412V (5 immature thalli, mesothorax), BR5020212165385V (1 mature thallus, right protibia), and BR5020212164357V (1 mature thallus, right mesofemur). Paratype: Belgium, Province Vlaams-Brabant, Meise, Domein van Bouchout, 50.92745N, 4.323917E, 32 m a.s.l., 30 Apr. 2020, leg. A. De Kesel, rivulet-associated grassland, on B. (P.) biguttatum, ADK6523 (BR), slide BR5020195033527V (2 mature thalli, mesosternum).

Etymology

From quarantena, which was used in 14th–15th century Venetian language for a forty-day isolation period. The new species was described during the 2020 quarantine period imposed to curb the spread of the COVID-19 virus.

Description

Thallus 300–465 µm long from foot to perithecial tip; colored hyaline at the lower receptacular cells (I and II) and the inner appendage, otherwise pigmented light to dark brown; especially the upper receptacular cells (III, IV and V), cell VI, and the perithecium darkening with age. Cell I elongated, usually straight, 56–107 × 22–33 µm; sometimes bent and then wider at the upper end. Cell II slender, mostly with parallel margins, longer than cell I, 73–160 × 29–40 µm, anterior margin shorter than posterior. Cells III and VI side by side, with septum II–III always much shorter than septum II–VI. Cell III with a narrow base, 29–43 µm long, widening upwards and then 22–29 µm wide at the apex. Cell VI more or less rectangular, 30–34 × 23–30 µm. Cell IV more or less rectangular, slightly broader than long, 20–32 × 25–30 µm. Cell V small, triangular, situated in the inner-upper corner of cell IV, 9–14 × 7–14 µm, as pigmented as surrounding cells. Insertion cell brownish black, flattened, barely marking a constriction on the posterior margin of the thallus, attached to the lower fifth of the posterior margin of the perithecial wall, 18–25 µm wide and 90–128 µm from the perithecial tip. Inner appendage hyaline, composed of 2–4(–6) short branches, rarely exceeding the perithecial tip, 88–150 µm long, resulting from successive dichotomies starting at the basal cell, the latter 9–14 × 6–12 µm. Antheridia short, flask-shaped, few in number, usually on the young inner appendage and arising laterally from its suprabasal cell. Outer appendage up to 250–335 µm long, extending beyond the perithecial tip, often entirely light brown, composed of 4–6(–8) branches, resulting from successive dichotomies starting at the suprabasal cell; the basal cell longer than broad, 23–32 × 15–21 µm, almost entirely hyaline. Perithecium ellipsoid, venter only very slightly asymmetrical, anterior and posterior margins almost equally convex, 109–157 × 43–64 µm, length/width ratio 1.9–2.5, widest in the middle; perithecial tip asymmetrical, with prominent and rounded posterior margin; preostiolar spots black, in older thalli merging into a pre-apical ring, always with distinctly paler zone under the posterior spot. Ascospores two-celled, hyaline, 59–65 × 4.2–5.5 µm, with slime sheath.

Material sequenced

Belgium, Province Vlaams Brabant, Meise, Domein van Bouchout, 50.9267056N, 4.3220028E, 30 m a.s.l., 26 Apr. 2019, leg. A. De Kesel, rivulet associated grassland, on Bembidion biguttatum (Coleoptera, Carabidae), ADK6448 (BR), isolate E13T12 (3 mature thalli, prothorax, LSU: MT371368).

Hosts and distribution

Thus far only known on Bembidion biguttatum from the type locality in Belgium. Reported as Laboulbenia sp. nov. in De Weggheleire (2019).

Notes

Morphologically, L. quarantenae mostly resembles L. vulgaris Peyr., but it differs from it by the very low position of the insertion cell (regardless of the origin of the thallus), the successive dichotomous branching of the outer appendage, the poorly pigmented to nearly hyaline basal cell of the outer appendage, and the slender habitus. Although these characters may vary to some extent, eventually resulting in specimens that are morphologically close to L. vulgaris, our LSU phylogeny (Figure 2) shows that sequences of typical L. vulgaris obtained from Carabidae known to host L. vulgarisBembidion tetracolum Say, 1823 and Ocys harpaloides (Audinet-Serville, 1821) (Santamaría et al. 1991; Majewski 1994; Haelewaters et al. 2019a; De Kesel et al. 2020)–fall in a monophyletic clade separated from L. quarantenae. The two isolates of L. vulgaris from B. tetracolum were collected in Belgium (isolate E10T2) and Latvia (isolate E11T6), from populations that are 1,550 km apart, but they were placed together among isolates from O. harpaloides (all from Belgium). Laboulbenia quarantenae, on the other hand, was collected between <1 and 21 km distance from where hosts of L. vulgaris were collected.

Figure 2. 

Maximum clade creditability tree of Laboulbenia isolates reconstructed from an LSU dataset, with L. bruchii as outgroup. The topology is the result of Bayesian inference performed with BEAST. For each node, ML BS (≥ 65) and Bayesian pp (≥ 0.7) are presented above/below the branch leading to that node. Isolates are color-coded by host; L. quarantenae sp. nov. is highlighted with gray shading.

Phylogenetically, L. quarantenae may be more closely related to L. flagellata than to L. vulgaris. Laboulb quarantenae and L. flagellata (sensu lato) were retrieved as sister taxa in our phylogeny, although no statistical support was retrieved for this sister relationship. Whereas species boundaries are evident based on our phylogeny, it goes without saying that both taxon sampling and sequence data need to be greatly expanded upon to resolve relationships among species of Laboulbenia. The new species is apparently very rare and was never found in combination with L. vulgaris, the more common parasite from Bembidion biguttatum in Belgium (De Kesel 1998; De Kesel et al. 2020).

Figure 3. 

Hesperomyces halyziae Haelew. & De Kesel from Halyzia sedecimguttata A mature thallus from slide D. Haelew. 955a, holotype B mature thallus from slide BR5020212156406V. Scale bar: 100 µm.

In Europe, many species of Laboulbenia have been reported on Bembidion Latreille, 1802 (Santamaría et al. 1991). Of those, L. pedicellata Thaxt. and L. vulgaris Peyr. are among the most reported ones. Bembidion biguttatum belongs to subfamily Trechinae. To our knowledge, this species is infected by either L. murmanica Huldén (S. Santamaría pers. comm.), L. pedicellata (Scheloske 1969; Majewski 1994), or L. vulgaris (Majewski 1994; De Kesel et al. 2020). Based on the position of its insertion cell as well as the morphology of both the outer appendage and the androstichum (cells II, IV, and V), L. quarantenae is fundamentally different from these three species. The outer appendage of L. quarantenae is reminiscent of the one from L. flagellata, which, however, is a more robust species reported from 80 genera of Carabidae belonging to Anthiinae, Brachininae, Elaphrinae, Harpalinae, Loricerinae, Nebriinae, and Patrobinae (but not Trechinae) (Santamaría et al. 1991; Santamaría 1998; Haelewaters et al. 2019a).

Figure 4. 

A–I Laboulbenia quarantena De Kesel & Haelew. from Bembidion biguttatum, specimen ADK6448: A mature thallus from prothorax, slide BR5020212163329V, holotype B mature thallus from prothorax with less pigmented perithecium C mature thallus from the right mesofemur D–F mature thalli from the right protibia G immature thallus from the prothorax H mature thallus from the right mesofemur I ascospores J–K laboulbenia vulgaris Peyr: J mature thallus from prothorax of Bembidion tetracolum, specimen ADK5557 K mature thallus from mesothorax of Ocys harpaloides, specimen ADK6353. One of the diagnostic characteristics of the new species–the positioning of the insertion cell–is shown in a mature thallus of L. quarantenae (E) and one of L. vulgaris (J). Scale bar: 100 µm.

Bembidion biguttatum, the host for L. quarantenae, belongs to the subgenus Philochtus. Representatives of Laboulbenia reported from Bembidion subgenus Philochtus are few and include two species only: L. pedicellata and L. vulgaris. Two thalli of Laboulbenia “sp. similar to L. vulgaris” from Bembidion bruxellense Wesmael, 1835 [as B. rupestre (Linnaeus, 1767) are illustrated in Majewski (1994: Pl. 53, Figs 1, 2). Their morphology comes close to L. quarantenae but cell V is much larger and the insertion cell is not situated low enough along the posterior margin of the perithecial wall. Also L. parvula is reported on subgenus Philochtus in Santamaría et al. (1991), but this species is much smaller (180–190 µm total length) compared to L. quarantenae, it has a deeply pigmented basal cell of the outer appendage, the inner and outer appendage each carry 4–8 very slender branches, and its perithecial tip is rather squarish.

As we explore patterns of speciation of taxa in both Herpomycetales and Laboulbeniales using integrative taxonomy, we can start linking some of these patterns to morphological or life history traits. One candidate trait is the haustorium–a rhizoidal structure that penetrates the host’s integument to make contact with the haemocoel, increasing surface area for nutrient uptake and providing holdfast. We hypothesize that – due to the invasive nature of their haustorium – Herpomycetales and haustorial Laboulbeniales, such as species of Hesperomyces, maintain close interactions with their hosts, possibly involving adaptations to the hosts’ defense systems and leading to escape-and-radiate coevolution (Ehrlich and Raven 1964). These developments result in an evolutionary arms race, with specialization and leading to speciation (One Host One Parasite model, Figure 1). While all 27 species of Herpomyces form multiple haustoria, not all Laboulbeniales penetrate their host. Recently, Tragust et al. (2016) presented evidence for four species of Laboulbeniales to be superficially attached to their host, and also L. flagellata and L. vulgaris do not seem to perforate their hosts. There are no strict developmental barriers for non-penetrating species and their ascospores may develop on multiple arthropods given that they co-occur in a given microhabitat, resulting in parasite species with more than one host (e.g., L. vulgaris in Figure 2), in contrast to the host-specific species of Hesperomyces. Undoubtedly, other factors come into play; more studies of speciation and species limits, specificity, host shifting, and transmission patterns are needed to test said hypothesis.

Alphabetical checklist of thallus-forming Laboulbeniomycetes in Belgium and the Netherlands

Herpomycetales

1. Herpomyces ectobiae Thaxt., Proc. Am. Acad. Arts Sci. 38(2): 20 (1902) [1903]

Blattella germanica (Linnaeus, 1767) (Blattodea, Ectobiidae) Be

2. Herpomyces periplanetae Thaxt., Proc. Am. Acad. Arts Sci. 38(2): 13 (1902) [1903]

Blatta orientalis Linnaeus, 1758 (Blattodea, Blattidae) Be

Periplaneta americana (Linnaeus, 1758) (Blattodea, Blattidae) Be

3. Herpomyces stylopygae Speg., Anal. Mus. Nac. Hist. Nat. B. Aires 29: 551 (1917)

Blatta orientalis Linnaeus, 1758 (Blattodea, Blattidae) Be

Laboulbeniales

4. Aphanandromyces audisioi W. Rossi, Mycologia 74: 522 (1982)

Brachypterus urticae (Fabricius, 1792) (Coleoptera, Kateretidae) Be

5. Asaphomyces tubanticus (Middelh. & Boelens) Scheloske, Parasitol. Schriftenr. 19: 92 (1969)

Catops fuliginosus Erichson, 1837 (Coleoptera, Leiodidae) Nl

Catops fuscus (Panzer, 1794) Be, Nl

Catops longulus Kellner, 1846 Be

Catops nigricans (Spence, 1813) Be, Nla

Catops sp. Be

Choleva sp. (Coleoptera, Leiodidae) Nl

a Fungus as Barbariella tubantica Middelh. & Boelens ex Middelh. in Middelhoek (1949).

6. Bordea denotata Haelew. & De Kesel, Nova Hedwig. 98: 114 (2014)

Bibloporus bicolor (Denny, 1825) (Coleoptera, Staphylinidae) Nl

7. Botryandromyces heteroceri (Thaxt.) I.I. Tav. & T. Majewski, Mycotaxon 3: 195 (1976)

Heterocerus fenestratus (Thunberg, 1784) (Coleoptera, Heteroceridae) Be

Heterocerus flexuosus Stephens, 1828 Be

Heterocerus hispidulus Kiesenwetter, 1843 Be

Heterocerus obsoletus Curtis, 1828 Nl

8. Cantharomyces denigratus Thaxt., Mem. Am. Acad. Arts Sci. 16: 27 (1931)

Dryops luridus (Erichson, 1847) (Coleoptera, Dryopidae) Be

9. Cantharomyces elongatus Haelew. & De Kesel, Mycotaxon 123: 468 (2013)

Syntomium aeneum (Müller, 1821) (Coleoptera, Staphylinidae) Nl

10. Cantharomyces italicus Speg., Anal. Mus. Nac. Hist. Nat. B. Aires 27: 42 (1915)

Dryops luridus (Erichson, 1847) (Coleoptera, Dryopidae) Be

11. Cantharomyces orientalis Speg., Anal. Mus. Nac. Hist. Nat. B. Aires 27: 43 (1915)

Carpelimus corticinus (Gravenhorst, 1806) (Coleoptera, Staphylinidae) Be, Nla

Carpelimus foveolatus (Sahlberg, 1832) Be

Carpelimus sp. Be

Diglotta mersa (Haliday, 1837) (Coleoptera, Staphylinidae) Be

a Host as Troglophloeus corticinus (Gravenhorst, 1806), fungus as Cantharomyces thaxteri Maire in Middelhoek (1949).

12. Cantharomyces platystethi Thaxt., Proc. Am. Acad. Arts Sci. 35: 415 (1900)

Platystethus sp. (Coleoptera, Staphylinidae) Be

13. Cantharomyces robustus T. Majewski, Acta Mycol. 23: 99 (1990) [1987]

Carpelimus bilineatus Stephens, 1834 (Coleoptera, Staphylinidae) Be

Carpelimus corticinus (Gravenhorst, 1806) Be

Carpelimus rivularis (Motschulsky, 1860) Be, Nl

Carpelimus sp. Be

Gnypeta rubrior Tottenham, 1939 (Coleoptera, Staphylinidae) Be

14. Chaetarthriomyces crassiappendicatus Scheloske

Chaetarthria seminulum (Herbst, 1797) (Coleoptera, Hydrophilidae) Nl

15. Chitonomyces aculeifer Speg., Anal. Mus. Nac. Hist. Nat. B. Aires 27: 44 (1915)

Graptodytes pictus (Fabricius, 1787) (Coleoptera, Dytiscidae) Be

Haliplus sp. (Coleoptera, Haliplidae) Be

16. Chitonomyces bidessarius (Thaxt.) Thaxt., Mem. Am. Acad. Arts Sci. 12: 292 (1902)

Hygrotus impressopunctatus (Schaller, 1783) (Coleoptera, Dytiscidae) Nl

17. Chitonomyces italicus Speg., Anal. Mus. Nac. Hist. Nat. B. Aires 27: 46 (1915)

Laccophilus hyalinus (De Geer, 1774) (Coleoptera, Dytiscidae) Be

18. Chitonomyces melanurus Peyr., Sitzber. Akad. Wiss. Wien Math.-Naturw. Kl. 68: 250 (1873)

Laccophilus hyalinus (De Geer, 1774) (Coleoptera, Dytiscidae) Be

Laccophilus minutus (Linnaeus, 1758) Nla

a New record: Utrecht Province, Soest, Soesterveen, 17 Oct. 1924, leg. F.C. Drescher, on Laccophilus minutus [as Laccophilus obscurus (Panzer, 1795)] (Naturalis Biodiversity Center), slide D. Haelew. 075a (BR-MYCO, 5 thalli, margin of left elytron).

19. Chitonomyces paradoxus (Peyr.) Thaxt., Mem. Am. Acad. Arts Sci. 12: 287 (1902)

Laccophilus hyalinus (De Geer, 1774) (Coleoptera, Dytiscidae) Be

Laccophilus minutus (Linnaeus, 1758) Nl

20. Compsomyces lestevae Thaxt., Proc. Am. Acad. Arts Sci. 35: 439 (1900)

Lesteva longoelytrata (Goeze, 1777) (Coleoptera, Staphylinidae) Be

Lesteva pubescens Mannerheim, 1830 Be

Lesteva sicula subsp. heeri Fauvel, 1871 Be, Nl

Lesteva sp. Be

21. Coreomyces arcuatus Thaxt., Mem. Am. Acad. Arts Sci. 16: 324 (1931)

Sigara striata (Linnaeus, 1758) (Hemiptera, Corixidae) Be

22. Corethromyces henrotii Balazuc [as ‘henroti’], Bull. Mens. Soc. Linn. Lyon 42: 283 (1973)

Choleva cisteloides (Frölich, 1799) (Coleoptera, Leiodidae) Be

Choleva fagniezi Jeannel, 1922 Nl

Choleva jeanneli Britten, 1922 Nl

Choleva oblonga Latreille, 1708 Nl

23. Corethromyces stilici Thaxt., Proc. Am. Acad. Arts Sci. 37: 42 (1901)

Rugilus (Rugilus) rufipes Germar, 1836 (Coleoptera, Staphylinidae) Be, Nla

Rugilus (Rugilus) similis (Erichson, 1839) Be

Rugilus sp. Be

a Host as Stilicus rufipes (Germar, 1836) in Middelhoek (1943a, 1945).

24. Cryptandromyces bibloplecti T. Majewski, Acta Mycol. 25: 43 (1990)

Pselaphinae gen et sp. indet. (Coleoptera, Staphylinidae) Be

25. Cryptandromyces elegans (Maire) W. Rossi & D. Castaldo, Pl. Biosystems 138: 264 (2004)

Brachygluta fossulata (Reichenbach, 1816) (Coleoptera, Staphylinidae) Nl

Brachygluta xanthoptera Reichenbach, 1816 Be

26. Cryptandromyces euplecti Santam., Nova Hedwig. 72: 384 (2001)

Euplectus sanguineus Denny, 1825 (Coleoptera, Staphylinidae) Be

27. Dimorphomyces myrmedoniae Thaxt., Proc. Am. Acad. Arts Sci. 36: 409 (1900) [1901]

Gnypeta rubrior Tottenham, 1939 (Coleoptera, Staphylinidae) Be

28. Diphymyces kaaistoepi Haelew. & De Kesel, Sterbeeckia 35: 63 (2019)

Choleva cisteloides (Frölich, 1799) (Coleoptera, Leiodidae) Be

Choleva fagniezi Jeannel, 1922 Nl

29. Distolomyces forficulae (T. Majewski) I.I. Tav., Mycol. Mem. 9: 207 (1985)

Forficula auricularia Linnaeus, 1758 (Dermaptera, Forficulidae) Be, Nl

30. Ecteinomyces trichopterophilus Thaxt., Proc. Am. Acad. Arts Sci. 38: 26 (1902) [1903]

Acrotrichis fascicularis (Herbst, 1793) (Coleoptera, Ptiliidae) Be

Acrotrichis grandicollis (Mannerheim, 1844) Nl

Acrotrichis intermedia (Gillmeister, 1845) Be

Acrotrichis sp. Be

31. Eucantharomyces stammeri Scheloske, Parasitol. Schriftenr. 19: 108 (1969)

Calathus melanocephalus (Linnaeus, 1758) (Coleoptera, Carabidae) Be

32. Euphoriomyces agathidii (Maire) I.I. Tav., Mycol. Mem. 9: 218 (1985)

Agathidium laevigatum Erichson, 1845 (Coleoptera, Leiodidae) Nla

a New record: Noord Brabant Province, Tilburg, nature reserve De Kaaistoep, 51.540672N 5.013867E, 3–17 Jun. 2000, leg. Working Group Insects of the Royal Dutch Natural History Association (KNNV), pitfall trap, ±2.5 m S of Quercus robur #2, on Agathidium laevigatum (NNKN), slides D. Haelew. 1064a (FH, 1 submature and 2 mature thalli, tip of left elytron) and D. Haelew. 1064b (NMBT, 1 juvenile and 2 mature thalli, tip of right elytron).

33. Euzodiomyces lathrobii Thaxt., Proc. Am. Acad. Arts Sci. 35: 449 (1900)

Lathrobium brunnipes (Fabricius, 1793) (Coleoptera, Staphylinidae) Be

Lathrobium elongatum (Linnaeus, 1767) Be, Nl

Lathrobium geminum Kraatz, 1857 Be, Nl

Lathrobium laevipenne Heer, 1839 Nl

Lathrobium sp. Be

Lobrathium multipunctum (Gravenhorst, 1802) (Coleoptera, Staphylinidae) Be

Patrobus atrorufus (Stroem, 1768) (Coleoptera, Carabidae) Be

Pterostichus strenuus (Panzer, 1796) (Coleoptera, Carabidae) Be

34. Fanniomyces burdigalensis Balazuc, Revue Mycol. 43: 402 (1979)

Copromyza stercoraria (Meigen, 1830) (Diptera, Sphaeroceridae) Bea

Crumomyia pedestris (Meigen, 1830) (Diptera, Sphaeroceridae) Bea

a Fungus as Stigmatomyces burdigalensis (Balazuc) A. Weir & W. Rossi in De Kesel et al. (2020).

35. Fanniomyces ceratophorus (Whisler) T. Majewski, Acta Mycol. 8: 230 (1972)

Fannia canicularis (Linnaeus, 1761) (Diptera, Fanniidae) Nla

a Fungus described as Stigmatomyces ceratophorus Whisler, and later recombined in Fanniomyces T. Majewski by Majewski (1972), based on the branching pattern of the primary appendage. Weir and Rossi (1995), in turn, found no valid rationale to maintain Fanniomyces as a separate genus and considered it a junior synonym of Stigmatomyces, stating that “the structure of the antheridial appendage is particularly variable”. However, based on an SSU–LSU ribosomal DNA dataset, Haelewaters et al. (in press) found that 1) Stigmatomyces as currently circumscribed is paraphyletic and 2) Fanniomyces is supported as a stand-alone genus with two species, F. burdigalensis and F. ceratophorus.

36. Haplomyces texanus Thaxt., Proc. Am. Acad. Arts Sci. 28: 160 (1893)

Bledius gallicus (Gravenhorst, 1806) (Coleoptera, Staphylinidae) Nla

a Host as Bledius fracticornis (Paykull, 1790) in Middelhoek (1943a).

37. Helodiomyces elegans F. Picard, Bull. Soc. Mycol. Fr. 29: 557 (1913)

Dryops anglicanus Edwards, 1909 (Coleoptera, Dryopidae) Nl

Dryops auriculatus (Geoffroy, 1785) Nl

Dryops luridus (Erichson, 1847) Be, Nl

38. Hesperomyces coccinelloides Thaxt., Mem. Am. Acad. Arts Sci. 16: 110 (1931)

Stethorus punctillum (Weise, 1891) (Coleoptera, Coccinellidae) Be

39. Hesperomyces halyziae Haelew. & De Kesel, sp. nov.

Halyzia sedecimguttata (Linnaeus, 1758) (Coleoptera, Coccinellidae) Bea, Nlb

a Fungus as Hesperomyces virescens Thaxt. sensu lato in De Kesel et al. (2020).

b Fungus as Hesperomyces virescens Thaxt. in Haelewaters and van Wielink (2016) and Haelewaters et al. (2017).

40. Hesperomyces virescens Thaxt., Proc. Am. Acad. Arts Sci. 25: 264 (1891), sensu lato

Harmonia axyridis (Pallas, 1773) (Coleoptera, Coccinellidae) Be, Nl

Tytthaspis sedecimpunctata (Linnaeus, 1761) (Coleoptera, Coccinellidae) Be

41. Hydraeomyces halipli (Thaxt.) Thaxt., Mem. Am. Acad. Arts Sci. 12: 294 (1902)

Haliplus flavicollis Sturm, 1834 (Coleoptera, Haliplidae) Nl

Haliplus immaculatus Gerhardt, 1877 Be

Haliplus lineatocollis (Marsham, 1802) Be

Haliplus lineolatus Mannerheim, 1844 Be

Haliplus ruficollis (De Geer, 1774) Be, Nl

Haliplus sp. Be

42. Hydrophilomyces cf. gracilis T. Majewski, Acta Mycol. 10: 272 (1974)

Cercyon marinus Thomson, 1853 (Coleoptera, Hydrophilidae) Be

Cercyon sp. Be

43. Hydrophilomyces cf. hamatus T. Majewski, Acta Mycol. 10: 274 (1974)

Cercyon marinus Thomson, 1853 (Coleoptera, Hydrophilidae) Be

44. Idiomyces peyritschii Thaxt., Proc. Am. Acad. Arts Sci. 28: 162 (1893)

Deleaster dichrous Gravenhorst, 1802 (Coleoptera, Staphylinidae) Be, Nl

45. Kainomyces rehmanii T. Majewski, Polish Bot. Stud. 1: 121 (1990)

Acrotrichis dispar (Matthews, 1865) (Coleoptera, Ptiliidae) Nl

Acrotrichis sp. Be

46. Laboulbenia acupalpi Speg., Anal. Mus. Nac. Hist. Nat. B. Aires 26: 458 (1915)

Acupalpus parvulus (Sturm, 1825) (Coleoptera, Carabidae) Nl

47. Laboulbenia anoplogenii Thaxt., Proc. Am. Acad. Arts Sci. 35: 156 (1899) [1899–1900]

Stenolophus mixtus (Herbst, 1784) (Coleoptera, Carabidae) Be, Nl

Stenolophus teutonus (Schrank, 1781) Be

48. Laboulbenia argutoris Cépède & F. Picard, Bull. Biol. Fr. Belg. 42: 260 (1909)

Pterostichus diligens (Sturm, 1824) (Coleoptera, Carabidae) Be

Pterostichus strenuus (Panzer, 1796) Be, Nl

Pterostichus vernalis (Panzer, 1796) Nl

49. Laboulbenia atlantica Thaxt., Mem. Am. Acad. Arts Sci. 12: 336 (1902)

Lobrathium multipunctum (Gravenhorst, 1802) (Coleoptera, Staphylinidae) Be

50. Laboulbenia aubryi Balazuc, Revue Mycol. 43: 393 (1979)

Amara aenea (De Geer, 1774) (Coleoptera, Carabidae) Bea

a New record: Belgium, Province Vlaams Brabant, Meise, Domein van Bouchout, 50.9274389N 4.323925E, ca. 25 m a.s.l., 6 Apr. 2020, leg. A. De Kesel, wet meadow, on Amara aenea, ADK6520 (BR), slides ADK6520a (BR-MYCO, 1 mature thallus, elytra) and ADK6520b (BR-MYCO, 2 immature and 4 mature thalli, elytra).

51. Laboulbenia barbara Middelh. & Boelens, Ned. Kruidk. Arch. 53: 99 (1943a)

Philonthus punctus (Gravenhorst, 1802) (Coleoptera, Staphylinidae) Nl

52. Laboulbenia benjaminii Balazuc ex Santam., Fl. Mycol. Iber. 4: 45 (1998)

Badister bullatus (Schrank, 1798) (Coleoptera, Carabidae) Be, Nla

Badister lacertosus Sturm, 1815 Be

Badister sodalis (Duftschmid, 1812) Be, Nlb

Badister unipustulatus Bonelli, 1813 Be

a Host as Badister bipustulatus (Fabricius, 1792), fungus as Laboulbenia polyphaga Thaxt. in Middelhoek (1949) and Meijer (1975).

b Fungus as Laboulbenia polyphaga Thaxt. in Meijer (1975).

53. Laboulbenia calathi T. Majewski, Polish Bot. Stud. 7: 89 (1994)

Calathus erratus (Sahlberg, 1827) (Coleoptera, Carabidae) Be

Calathus fuscipes (Goeze, 1777) Nl

Calathus melanocephalus (Linnaeus, 1758) Be, Nl

54. Laboulbenia clivinalis Thaxt., Proc. Am. Acad. Arts Sci. 35: 155 (1899) [1899–1900]

Clivina collaris (Herbst, 1784) (Coleoptera, Carabidae) Be

Clivina fossor (Linnaeus, 1758) Be, Nl

55. Laboulbenia collae T. Majewski, Polish Bot. Stud. 7: 104 (1994)

Agonum micans (Nicolai, 1822) (Coleoptera, Carabidae) Be

Paranchus albipes (Fabricius, 1796) (Coleoptera, Carabidae) Be, Nl

56. Laboulbenia coneglianensis Speg., Redia 10: 47 (1914)

Harpalus affinis (Schrank, 1781) (Coleoptera, Carabidae) Be, Nla

Harpalus atratus Latreille, 1804 Be

Harpalus attenuatus Stephens, 1828 Be

Harpalus griseus (Panzer, 1796) Be, Nlb

Harpalus rufipes (De Geer, 1774) Be

Harpalus tardus (Panzer, 1796) Be, Nl

Harpalus sp. Be

Ophonus rufibarbis (Fabricius, 1792) (Coleoptera, Carabidae) Be

Parophonus maculicornis (Duftschmid, 1812) (Coleoptera, Carabidae) Nlc

a Host as Harpalus aeneus (Fabricius, 1775), fungus as Laboulbenia elongata Thaxt. in Middelhoek (1949).

b Host as Pseudophonus griseus (Panzer, 1796), fungus as Laboulbenia elongata Thaxt. in Middelhoek (1949).

c Fungus as Laboulbenia melanaria Thaxt. in Haelewaters et al. (2012a).

57. Laboulbenia cristata Thaxt., Proc. Am. Acad. Arts Sci. 29: 174 (1893)

Paederus fuscipes Curtis, 1826 (Coleoptera, Staphylinidae) Nl

Paederus littoralis Gravenhorst, 1802 Be

Paederus riparius (Linnaeus, 1758) Be, Nl

Paederus sp. Be

58. Laboulbenia dubia Thaxt., Proc. Am. Acad. Arts Sci. 38: 35 (1902) [1903]

Philonthus cognatus Stephens, 1832 (Coleoptera, Staphylinidae) Be

59. Laboulbenia egens Speg., Anal. Soc. Cient. Argent. 85: 323 (1918)

Elaphropus parvulus (Dejean, 1831) (Coleoptera, Carabidae) Be

Paratachys micros (Fischer von Waldheim, 1828) (Coleoptera, Carabidae) Be

60. Laboulbenia elaphri Speg., Anal. Mus. Nac. B. Aires 26: 64 (1915)

Elaphrus cupreus Duftschmid, 1812 (Coleoptera, Carabidae) Be

Elaphrus riparius (Linnaeus, 1758) Be

61. Laboulbenia eubradycelli Huldén, Karstenia 25: 4 (1985)

Bradycellus harpalinus (Audinet-Serville, 1821) (Coleoptera, Carabidae) Be, Nl

Bradycellus ruficollis (Stephens, 1828) Be

Bradycellus verbasci (Duftschmid, 1812) Be, Nl

Trichocellus placidus (Gyllenhal, 1827) (Coleoptera, Carabidae) Be

62. Laboulbenia fasciculata Peyr., Sitzber. Akad. Wiss. Wien Math.-naturw. Kl. 68: 248 (1873)

Nebria brevicollis (Fabricius, 1792) (Coleoptera, Carabidae) Be

Omophron limbatum (Fabricius, 1777) (Coleoptera, Carabidae) Be, Nla

Patrobus atrorufus (Stroem, 1768) (Coleoptera, Carabidae) Be

Pterostichus nigrita (Paykull, 1790) (Coleoptera, Carabidae) Be

a New record: No locality, no date, on Omophron limbatum (Naturalis Biodiversity Center), slide D. Haelew. 074a (BR-MYCO, 3 thalli, left metatibia).

63. Laboulbenia fennica Huldén, Karstenia 23: 54 (1983)

Gyrinus marinus Gyllenhal, 1808 (Coleoptera, Gyrinidae) Nl

Gyrinus substriatus Stephens, 1829 Be, Nl

64. Laboulbenia filifera Thaxt., Proc. Am. Acad. Arts Sci. 28: 165 (1893)

Harpalus affinis (Schrank, 1781) (Coleoptera, Carabidae) Nla

a Host as Harpalus aeneus (Fabricius, 1775) in Middelhoek (1949). The microscope slide from the collection of W.J. Kossen was reported to be in very poor condition; as a result, no illustrations could be made (Middelhoek 1949). For the time being, we retain the identification of the fungus. Laboulbenia filifera was described on a species of Anisodactylus Dejean, 1829 (Coleoptera, Carabidae) in the USA, and it is possible that European records of L. filifera belong in L. flagellata (Majewski 1994, Haelewaters et al. 2019a). The species is not included in the identification key.

65. Laboulbenia flagellata Peyr., Sitzber. Akad. Wiss. Wien Math.-naturw. Kl. 68: 247 (1873), sensu lato

Agonum emarginatum (Gyllenhal, 1827) (Coleoptera, Carabidae) Be

Acupalpus flavicollis (Sturm, 1825) Nla

Agonum fuliginosum (Panzer, 1809) Be, Nlb

Agonum marginatum (Linnaeus, 1758) Be, Nl

Agonum micans (Nicolai, 1822) Be

Agonum moestum (Duftschmid, 1812) Be, Nla

Agonum muelleri (Herbst, 1784) Be, Nl

Agonum nigrum Dejean, 1828 Be

Agonum thoreyi Dejean, 1828 Be, Nl

Agonum viduum (Panzer, 1796) Nl

Agonum viridicupreum Goeze, 1777 Be

Anchomenus dorsalis (Pontoppidan, 1763) (Coleoptera, Carabidae) Nlc

Anisodactylus binotatus (Fabricius, 1787) (Coleoptera, Carabidae) Be

Laemostenus terricola (Herbst, 1784) (Coleoptera, Carabidae) Be

Limodromus assimilis (Paykull, 1790) (Coleoptera, Carabidae) Be, Nld

Loricera pilicornis (Fabricius, 1775) (Coleoptera, Carabidae) Be

Nebria brevicollis (Fabricius, 1792) (Coleoptera, Carabidae) Be

Oxypselaphus obscurus (Herbst, 1784) (Coleoptera, Carabidae) Be

Paranchus albipes (Fabricius, 1796) (Coleoptera, Carabidae) Be, Nle

Parophonus maculicornis (Duftschmid, 1812) Be

Pterostichus vernalis (Panzer, 1796) Be

Trichotichnus laevicollis (Duftschmid, 1812) (Coleoptera, Carabidae) Be

a Fungus as Laboulbenia elongata Thaxt. in Middelhoek (1949).

b Host as Europhilus fuliginosus (Panzer, 1809), fungus as Laboulbenia elongata Thaxt. in Middelhoek (1949).

c Host as Platynus dorsalis (Pontoppidan, 1763) in Zaneveld (1938), as Agonum dorsale (Pontoppidan, 1763) in Meijer (1975).

d Host as Platynus assimilis (Paykull, 1790) in Zaneveld (1938).

e Host as Platynus ruficornis (Goeze, 1777) in Zaneveld (1938).

66. Laboulbenia giardii Cépède & F. Picard, Bull. Sci. Fr. Belg. 42: 258 (1908)

Dicheirotrichus gustavii Crotch, 1871 (Coleoptera, Carabidae) Be, Nla

Dicheirotrichus obsoletus (Dejean, 1829) Be

a Host as Dicheirotrichus pubescens (Paykull, 1790) in Meijer (1975).

67. Laboulbenia gyrinicola Speg., Redia 10: 34 (1914)

Gyrinus marinus Gyllenhal, 1808 (Coleoptera, Gyrinidae) Be, Nl

Gyrinus natator (Linnaeus, 1758) Be

Gyrinus substriatus Stephens, 1829 Nl

68. Laboulbenia hyalopoda De Kesel, Sterbeeckia 18: 17 (1998)

Paradromius linearis (Olivier, 1795) (Coleoptera, Carabidae) Be

69. Laboulbenia inflata Thaxt., Proc. Am. Acad. Arts Sci. 27: 41 (1892)

Acupalpus dubius Schilsky, 1888 (Coleoptera, Carabidae) Be, Nl

Acupalpus exiguus Dejean, 1829 Be

Acupalpus parvulus (Sturm, 1825) Nl

Stenolophus mixtus (Herbst, 1784) (Coleoptera, Carabidae) Be

70. Laboulbenia kajanensis Huldén, Karstenia 23: 56 (1983)

Pterostichus diligens (Sturm, 1824) (Coleoptera, Carabidae) Be

Pterostichus strenuus (Panzer, 1796) Be

71. Laboulbenia lecoareri (Balazuc) Huldén, Karstenia 25: 6 (1985)

Trechoblemus micros (Herbst, 1784) (Coleoptera, Carabidae) Be

72. Laboulbenia leisti J. Siemaszko & Siemaszko, Polsk. Pism. Entomol. 6: 203 (1928) [1927]

Agonum muelleri (Herbst, 1784) (Coleoptera, Carabidae) Be

Leistus ferrugineus (Linnaeus, 1758) (Coleoptera, Carabidae) Be, Nl

73. Laboulbenia lichtensteinii F. Picard, Bull. Sci. Fr. Belg. 50: 449 (1917) [1916–1917]

Cillenus lateralis Samouelle, 1819 (Coleoptera, Carabidae) Nl

74. Laboulbenia littoralis De Kesel & Haelew., Mycologia 106: 408 (2014)

Cafius xantholoma (Gravenhorst, 1806) (Coleoptera, Staphylinidae) Be, Nl

75. Laboulbenia luxurians Peyr., Sitzber. Akad. Wiss. Wien Math.-naturw. Kl. 68: 248 (1873)

Bembidion dentellum (Thunberg, 1787) (Coleoptera, Carabidae) Nl

76. Laboulbenia metableti Scheloske, Parasitol. Schriftenr. 19: 124 (1969)

Syntomus foveatus (Geoffroy, 1785) (Coleoptera, Carabidae) Be, Nla

Syntomus truncatellus (Linnaeus, 1760) Be, Nla

a New records: Noord-Holland Province, Zuid-Kennemerland National Park, 31 Oct. 2016, leg. M. Boeken, pitfall trap, on Syntomus truncatellus, slide D. Haelew. 1236b (GENT, 2 juvenile thalli, pronotum). Ibid., 5 Jun. 2017, leg. M. Boeken, pitfall trap, on Syntomus truncatellus, slide D. Haelew. 1378a (GENT, 2 mature thalli, posterior margin of right elytron). Ibid., 5 Jun. 2017, leg. M. Boeken, pitfall trap, on Syntomus foveatus, slide D. Haelew. 1387a (GENT, 1 mature thallus, left elytron). Ibid., 5 Jun. 2017, leg. M. Boeken, pitfall trap, on Syntomus foveatus, slides D. Haelew. 1391a (FH, 5 mature thalli, right elytron), D. Haelew. 1391b (FH, 1 mature thallus, left metatrochanter), and D. Haelew. 1391c (FH, 1 submature and 2 mature thalli, mesocoxae). Ibid., 17 Jul. 2017, leg. M. Boeken, pitfall trap, on Syntomus truncatellus, slide D. Haelew. 1379a (GENT, 2 juvenile thalli, left elytron).

77. Laboulbenia murmanica Huldén, Karstenia 23: 57 (1983)

Bembidion assimile Gyllenhal, 1810 (Coleoptera, Carabidae) Be

78. Laboulbenia notiophili Cépède & F. Picard, Bull. Biol. Fr. Belg. 42: 259 (1909)

Demetrias atricapillus (Linnaeus, 1758) (Coleoptera, Carabidae) Be

Demetrias imperialis (Germar, 1824) Be

Demetrias monostigma Leach, 1819 Be

Notiophilus biguttatus (Fabricius, 1779) (Coleoptera, Carabidae) Be, Nl

Notiophilus rufipes Curtis, 1829 Be

Notiophilus substriatus Waterhouse, 1833 Nl

Notiophilus sp. Be

Paradromius linearis (Olivier, 1795) (Coleoptera, Carabidae) Be, Nla

Philorhizus melanocephalus (Dejean, 1825) (Coleoptera, Carabidae) Nl

a Fungus as Laboulbenia casnoniae Thaxt. in Haelewaters et al. (2012a).

79. Laboulbenia ophoni Thaxt., Proc. Am. Acad. Arts Sci. 35: 190 (1899) [1899–1900]

Harpalus rubripes (Duftschmid, 1812) (Coleoptera, Carabidae) Be

Ophonus rufibarbis (Fabricius, 1792) (Coleoptera, Carabidae) Be

80. Laboulbenia pedicellata Thaxt., Proc. Am. Acad. Arts Sci. 29: 109 (1893)

Bembidion aeneum Germar, 1824 (Coleoptera, Carabidae) Be, Nl

Bembidion articulatum (Panzer, 1796) Nl

Bembidion biguttatum (Fabricius, 1779) Nl

Bembidion gilvipes Sturm, 1825 Be

Bembidion guttula (Fabricius, 1792) Be, Nl

Bembidion iricolor Bedel, 1879 Be, Nl

Bembidion lunulatum (Geoffroy, 1785) Be, Nl

Bembidion minimum (Fabricius, 1792) Be, Nl

Bembidion normannum Dejean, 1831 Be, Nl

Bembidion obtusum Audinet-Serville, 1821 Be

Bembidion quadrimaculatum (Linnaeus, 1760) Be, Nl

Bembidion ustulatum (Linnaeus, 1758) Nl

Bembidion varium (Olivier, 1795) Be, Nl

Dyschirius globosus (Herbst, 1784) (Coleoptera, Carabidae) Nl

Dyschirius salinus Schaum, 1843 Nl

Dyschirius thoracicus (P. Rossi, 1790) Nla

Dyschirius tristis Stephens, 1827 Be

Dyschirius sp. Nl

Pogonus chalceus (Marsham, 1802) (Coleoptera, Carabidae) Be, Nl

a Host as Dyschirius arenosus Stephens, 1827 in Middelhoek (1943a).

81. Laboulbenia philonthi Thaxt., Proc. Am. Acad. Arts Sci. 28: 174 (1893)

Philonthus micans (Gravenhorst, 1802) (Coleoptera, Staphylinidae) Nl

Philonthus rubripennis Stephens, 1832 (Coleoptera, Staphylinidae) Be

Philonthus sp. Be

82. Laboulbenia pseudomasei Thaxt., Proc. Am. Acad. Arts Sci. 35: 196 (1899)

Loricera pilicornis (Fabricius, 1775) (Coleoptera, Carabidae) Be

Nebria brevicollis (Fabricius, 1792) (Coleoptera, Carabidae) Be

Pterostichus anthracinus (Panzer, 1795) (Coleoptera, Carabidae) Be

Pterostichus melanarius (Illiger, 1798) Nla

Pterostichus minor (Gyllenhal, 1827) Be

Pterostichus nigrita (Paykull, 1790) Be

Pterostichus strenuus (Panzer, 1796) Be

Stomis pumicatus (Panzer, 1796) (Coleoptera, Carabidae) Be

a New record: Drenthe Province, Oude Willem, 52.897438N 6.323432E, 2 Jun. 2014, leg. A.J. Dees, on Pterostichus melanarius (NNKN), slides D. Haelew. 1013a (FH, 1 juvenile thallus, right elytron) and D. Haelew. 1013b (FH, 1 submature thallus, prosternum).

83. Laboulbenia quarantenae De Kesel & Haelew, sp. nov.

Bembidion (Philochtus) biguttatum (Fabricius, 1779) (Coleoptera, Carabidae) Be

84. Laboulbenia rougetii Mont. & C.P. Robin, in Robin, Histoire Naturelle des végétaux parasites qui croissent sur l’homme et sur les animaux vivants (Paris): 622 (1853)

Brachinus crepitans (Linnaeus, 1758) (Coleoptera, Carabidae) Be

85. Laboulbenia slackensis Cépède & F. Picard, Compt. Rend. Assoc. Franç. Avancem. Sci. 35: 775 (1907)

Pogonus chalceus (Marsham, 1802) (Coleoptera, Carabidae) Be, Nl

86. Laboulbenia stilicicola Speg., Redia 10: 41 (1914)

Rugilus orbiculatus (Paykull, 1789) (Coleoptera, Staphylinidae) Be, Nla

Rugilus rufipes Germar, 1836 (Coleoptera, Staphylinidae) Be, Nlb

a Host as Stilicus orbiculatus (Paykull, 1789), fungus as Laboulbenia subterranea Thaxt. in Middelhoek (1943a, 1947a).

b Host as Stilicus rufipes Germar, 1836, fungus as Laboulbenia subterranea Thaxt. in Middelhoek (1943a, 1945).

87. Laboulbenia thaxteri Cépède & F. Picard, Bull. Biol. Fr. Belg. 42: 260 (1909)

Asaphidion flavipes (Linnaeus, 1760) (Coleoptera, Carabidae) Be

88. Laboulbenia vulgaris Peyr., Sitzber. Akad. Wiss. Wien Math.-naturw. Kl. 68: 248 (1873)

Asaphidion flavipes (Linnaeus, 1760) (Coleoptera, Carabidae) Nl

Bembidion assimile Gyllenhal, 1810 (Coleoptera, Carabidae) Nl

Bembidion biguttatum (Fabricius, 1779) Be, Nl

Bembidion bruxellense Wesmael, 1835 Nla

Bembidion dentellum (Thunberg, 1787) Be, Nl

Bembidion elongatum Dejean, 1831 Be

Bembidion femoratum Sturm, 1825 Be, Nl

Bembidion iricolor Bedel, 1879 Nl

Bembidion mannerheimi Sahlberg, 1827 Be

Bembidion minimum (Fabricius, 1792) Nl

Bembidion normannum Dejean, 1831 Nl

Bembidion pallidipenne (Illiger, 1802) Nl

Bembidion properans (Stephens, 1828) Be, Nl

Bembidion stephensii Crotch, 1866 Be

Bembidion testaceum (Duftschmid, 1812) Nl

Bembidion tetracolum Say, 1823 Be, Nl

Bembidion tibiale (Duftschmid, 1812) Be

Bembidion ustulatum (Linnaeus, 1758) Nl

Bembidion sp. Be

Dyschirius globosus (Herbst, 1784) (Coleoptera, Carabidae) Nl

Dyschirius salinus Schaum, 1843 Nl

Ocys harpaloides (Audinet-Serville, 1821) (Coleoptera, Carabidae) Be

Trechus quadristriatus (Schrank, 1781) (Coleoptera, Carabidae) Be

Trechus rubens (Fabricius, 1792) Be

a Host as Bembidion rupestre (Linnaeus, 1767) in Meijer (1975).

89. Mimeomyces zeelandicus Middelh. & Boelens, Ned. Kruidk. Arch. 53: 102 (1943)

Heterothops binotatus (Gravenhorst, 1802) (Coleoptera, Staphylinidae) Nl

90. Misgomyces dyschirii Thaxt., Proc. Am. Acad. Arts Sci. 35: 443 (1900)

Dyschirius aeneus (Dejean, 1825) (Coleoptera, Carabidae) Be, Nl

Dyschirius globosus (Herbst, 1784) Be, Nl

Dyschirius intermedius Putzeys, 1846 Be

Dyschirius politus (Dejean, 1825) Nl

Dyschirius salinus Schaum, 1843 Nl

Dyschirius tristis Stephens, 1827 Be, Nla

a Host as Dyschirius luedersi Wagner, 1915 in Middelhoek (1943a).

91. Monoicomyces bolitocharae T. Majewski, Polish Bot. Stud. 7: 193 (1994)

Bolitochara obliqua Erichson, 1837 (Coleoptera, Staphylinidae) Be

92. Monoicomyces britannicus Thaxt., Proc. Am. Acad. Arts Sci. 35: 412 (1900)

Acrotona fungi (Gravenhorst, 1806) (Coleoptera, Staphylinidae) Bea

Acrotona orbata (Erichson, 1837) Beb

Acrotona pseudotenera (Cameron, 1933) Nl

Atheta sp. (Coleoptera, Staphylinidae) Be

a Host as Atheta (Mocyta) fungi (Gravenhorst, 1806) in De Kesel et al. (2020).

b Host as Atheta (Mocyta) orbata (Erichson, 1837) in De Kesel et al. (2020).

93. Monoicomyces californicus (Thaxt.) Thaxt., Mem. Am. Acad. Arts Sci. 16: 38 (1931)

Anotylus sculpturatus (Gravenhorst, 1806) (Coleoptera, Staphylinidae) Be, Nla

a Host as Oxytelus sculpturatus Gravenhorst, 1806 in Middelhoek (1943a).

94. Monoicomyces fragilis Scheloske, Parasitol. Schriftenr. 19: 138 (1969)

Ocalea picata (Stephens, 1832) (Coleoptera, Staphylinidae) Be

95. Monoicomyces homalotae Thaxt., Proc. Am. Acad. Arts Sci. 35: 412 (1900)

Atheta aeneicollis (Sharp, 1869) (Coleoptera, Staphylinidae) Nl

Atheta amicula (Stephens, 1832) Nl

Atheta crassicornis (Fabricius, 1792) Nl

Atheta gagatina (Baudi, 1848) Nl

Atheta longicornis (Gravenhorst, 1802) Be

Atheta triangulum (Kraatz, 1856) Be, Nl

Atheta vestita (Gravenhorst, 1806) Be

Atheta xanthopus (Thomson, 1856) Nl

Atheta sp. Be

96. Monoicomyces invisibilis Thaxt., Proc. Am. Acad. Arts Sci. 36: 414 (1900) [1901]

Anotylus sculpturatus (Gravenhorst, 1806) (Coleoptera, Staphylinidae) Be

Anotylus sp. Be

Oxytelus laqueatus (Marsham, 1802) (Coleoptera, Staphylinidae) Be

Oxytelus sp. Be

Platystethus arenarius (Geoffroy, 1785) (Coleoptera, Staphylinidae) Be

97. Monoicomyces matthiatis T. Majewski, Acta Mycol. 25: 49 (1990) [1989]

Platystethus cf. arenarius (Geoffroy, 1785) (Coleoptera, Staphylinidae) Be

98. Monoicomyces myllaenae Santam., Nova Hedwig. 82: 358 (2006)

Myllaena elongata (Matthews, 1838) (Coleoptera, Staphylinidae) Nl

99. Monoicomyces nigrescens Thaxt., Proc. Am. Acad. Arts Sci. 35: 412 (1900)

Atheta atramentaria (Gyllenhal, 1810) (Coleoptera, Staphylinidae) Nl

Atheta sp. Be

Brundinia marina (Mulsant & Rey, 1853) (Coleoptera, Staphylinidae) Bea

Dilacra luteipes (Erichson, 1837) (Coleoptera, Staphylinidae) Nlb

a Host as Atheta (Actophylla) marina (Mulsant & Rey, 1853) in De Kesel et al. (2020).

b Host as Atheta luteipes (Erichson, 1837) in Middelhoek (1943a).

100. Peyritschiella biformis (Thaxt.) I.I. Tav., Mycol. Mem. 9: 270 (1985)

Philonthus umbratilis (Gravenhorst, 1802) (Coleoptera, Staphylinidae) Be

101. Peyritschiella dubia (Thaxt.) I.I. Tav., Mycol. Mem. 9: 270 (1985)

Philonthus politus (Linnaeus, 1758) (Coleoptera, Staphylinidae) Be

102. Peyritschiella furcifera (Thaxt.) I.I. Tav., Mycol. Mem. 9: 270 (1985)

Philonthus albipes (Gravenhorst, 1802) (Coleoptera, Staphylinidae) Nla

Philonthus rectangulus Sharp, 1874 Nla

a Fungus as Dichomyces furciferus Thaxt. in Middelhoek (1943a).

103. Peyritschiella heinemanniana De Kesel, Belg. J. Bot. 131: 177 (1999) [1998]

Xantholinus longiventris Heer, 1839 (Coleoptera, Staphylinidae) Be

104. Peyritschiella princeps (Thaxt.) I.I. Tav., Mycol. Mem. 9: 270 (1985)

Bisnius cephalotes (Gravenhorst, 1802) (Coleoptera, Staphylinidae) Be, Nla

Bisnius sordidus (Gravenhorst, 1802) Be, Nlb

Bisnius subuliformis (Gravenhorst, 1802) Nl

Philonthus politus (Linnaeus, 1758) (Coleoptera, Staphylinidae) Be

Philonthus varians (Paykull, 1789) Nlc

Philonthus sp. Be

a Host as Philonthus cephalotes (Gravenhorst, 1802), fungus as Dichomyces vulgatus Thaxt. in Middelhoek (1943a, 1947a).

b Host as Philonthus sordidus (Gravenhorst, 1802), fungus as Dichomyces princeps Thaxt. in Middelhoek (1941, 1943a, 1943b, 1943c), fungus also as Dichomyces vulgatus Thaxt. (variety sensu Thaxter 1908: 252) in Middelhoek (1943a, 1943b).

c Fungus as Dichomyces princeps Thaxt. in Middelhoek (1941).

105. Peyritschiella protea Thaxt., Proc. Am. Acad. Arts Sci. 35: 427 (1900)

Anotylus insecatus Gravenhorst, 1806 (Coleoptera, Staphylinidae) Be

Anotylus rugosus (Fabricius, 1775) Be, Nla

Anotylus sp. Be

Staphylinidae sp. indet. (Coleoptera, Staphylinidae) Be

a Host as Oxytelus rugosus (Fabricius, 1775) in Middelhoek (1943a, 1947a).

106. Peyritschiella vulgata (Thaxt.) I.I. Tav., Mycol. Mem. 9: 271 (1985)

Philonthus albipes (Gravenhorst, 1802) (Coleoptera, Staphylinidae) Nla

a Fungus as Dichomyces vulgatus Thaxt. in Middelhoek (1943b, 1943c).

107. Phaulomyces simplocariae De Kesel, Mycotaxon 50: 192 (1994)

Simplocaria semistriata Fabricius, 1794 (Coleoptera, Byrrhidae) Be

108. Rhachomyces canariensis Thaxt., Proc. Am. Acad. Arts Sci. 35: 436 (1900)

Trechus obtusus Erichson, 1837 (Coleoptera, Carabidae) Be, Nla

Trechus quadristriatus (Schrank, 1781) Be

Trechus sp. Be

a New record: Noord-Holland Province, Zuid-Kennemerland National Park, 17 Oct. 2016, leg. M. Boeken, pitfall trap, on Trechus obtusus Erichson, 1837 (Coleoptera, Carabidae), slides D. Haelew. 1242a (GENT, 9 thalli, right margin of pronotum) and D. Haelew. 1242b (GENT, 3 juvenile thalli, elytra). Ibid., 5 Jun. 2017, leg. M. Boeken, pitfall trap, on Trechus obtusus, slide D. Haelew. 1388a (GENT, 1 submature thallus, tip of left elytron).

109. Rhachomyces furcatus (Thaxt.) Thaxt., Proc. Am. Acad. Arts Sci. 30: 467 (1895) [1894]

Othius punctulatus (Goeze, 1777) (Coleoptera, Staphylinidae) Be

Othius subuliformis Stephens, 1833 Bea, Nl

a Host as Othius myrmecophilus Kiesenwetter, 1843 in De Kesel et al. (2020).

110. Rhachomyces lasiophorus (Thaxt.) Thaxt., Proc. Am. Acad. Arts Sci. 30: 468 (1895) [1894]

Acupalpus dubius Schilsky, 1888 (Coleoptera, Carabidae) Be

Acupalpus exiguus Dejean, 1829 Be, Nl

Anthracus consputus (Duftschmid, 1812) (Coleoptera, Carabidae) Nl

111. Rhachomyces philonthinus Thaxt., Proc. Am. Acad. Arts Sci. 35: 435 (1900)

Bisnius fimetarius (Gravenhorst, 1802) (Coleoptera, Staphylinidae) Be, Nla

Philonthus cruentatus (Gmelin, 1790) (Coleoptera, Staphylinidae) Nlb

Philonthus fumarius (Gravenhorst, 1806) Be

Philonthus marginatus (Müller, 1764) Be, Nl

Philonthus rectangulus Sharp, 1874 Be

Philonthus varians (Paykull, 1789) Be, Nlb

Philonthus sp. Be

a Host as Philonthus fimetarius (Gravenhorst, 1802) in Middelhoek (1943a, 1943d).

b Fungus as Rhachomycesphilonthi’ Thaxt. in Middelhoek (1943b).

112. Rhachomyces pilosellus (C.P. Robin) Thaxt., Proc. Am. Acad. Arts Sci. 30: 467 (1895) [1894]

Lathrobium fulvipenne (Gravenhorst, 1806) (Coleoptera, Staphylinidae) Be

Lathrobium geminum Kraatz, 1857 Be

113. Rhachomyces spinosu s Santam. & A.D. Cuesta-Segura, Nova Hedwig. 110: 362 (2020)

Syntomus foveatus (Geoffroy, 1785) (Coleoptera, Carabidae) Bea

a Fungus as Rhachomyces sciakyi W. Rossi in De Kesel et al. (2020)

114. Rhachomyces tenenbaumii J. Siemaszko & Siemaszko, Polsk. Pism. Entomol. 6: 205 (1928)

Thalassophilus longicornis (Sturm, 1825) (Coleoptera, Carabidae) Be

115. Rhadinomyces cristatus Thaxt., Proc. Am. Acad. Arts Sci. 28: 180 (1893)

Lathrobium brunnipes (Fabricius, 1793) (Coleoptera, Staphylinidae) Be

Lathrobium castaneipenne Kolenati, 1846 Be

Lathrobium elongatum (Linnaeus, 1767) Be

Lathrobium fulvipenne (Gravenhorst, 1806) Be

Lathrobium geminum Kraatz, 1857 Be

Lathrobium sp. Be

116. Rhadinomyces pallidus Thaxt., Proc. Am. Acad. Arts Sci. 28: 180 (1893)

Lathrobium elongatum (Linnaeus, 1767) (Coleoptera, Staphylinidae) Nl

117. Rhynchophoromyces anacaenae Scheloske, Parasitol. Schriftenr. 19: 143 (1969)

Anacaena lutescens (Stephens, 1829) (Coleoptera, Hydrophilidae) Be

118. Rickia dendroiuli W. Rossi, Rev. Mycol. 41: 531 (1977)

Julida sp. indet. Be

119. Rickia laboulbenioides De Kesel, Sterbeeckia 32: 6 (2013)

Cylindroiulus latestriatus (Curtis, 1845) (Julida, Julidae) Be, Nl

Cylindroiulus punctatus Leach, 1814 Be

Julida sp. indet. Be

120. Rickia peyerimhoffii Maire, Bull. Sci. Fr. Belg. 7: 290 (1916)

Scaphisoma sp. (Coleoptera, Staphylinidae) Be

121. Rickia proteini T. Majewski, Acta Mycol. 19: 191 (1985)

Proteinus sp. (Coleoptera, Staphylinidae) Be

122. Rickia wasmannii Cavara, Malpighia 13: 182 (1899)

Myrmica ruginodis Nylander, 1846 (Hymenoptera, Formicidae) Nl

Myrmica sabuleti Meinert, 1861 (Hymenoptera, Formicidae) Be, Nla

Myrmica scabrinodis Nylander, 1846 Nl

a Host as Myrmica scabrinodis Nylander, 1846 in Haelewaters (2012).

123. Siemaszkoa fennica Huldén, Karstenia 23: 63 (1983)

Ptenidium formicetorum Kraatz, 1851 (Coleoptera, Ptiliidae) Nl

124. Siemaszkoa ptenidii (Scheloske) I.I. Tav. & T. Majewski, Mycotaxon 3: 204 (1976)

Ptenidium sp. (Coleoptera, Ptiliidae) Be

125. Stichomyces conosomatis Thaxt., Proc. Am. Acad. Arts Sci. 37: 38 (1901)

Sepedophilus marshami (Stephens, 1832) (Coleoptera, Staphylinidae) Be

Sepedophilus nigripennis (Stephens, 1832) Be, Nl

Sepedophilus pedicularius (Gravenhorst, 1802) Be

Sepedophilus testaceus (Fabricius, 1792) Nl

Sepedophilus sp. Be

126. Stigmatomyces baeri H. Karst., Chemismus Pfl.-Zelle: 78 (1869)

• “Fannia canicularis” (Linnaeus, 1761) (Diptera, Fanniidae) Nla

a Host as Homalomyia canicularis (Linnaeus, 1761) in Boedijn (1923). The host identification may have been incorrect; Fannia canicularis is typically associated with Fanniomyces ceratophorus Whisler, whereas S. baeri is typically found on Musca domestica Linnaeus, 1758 (Diptera, Muscidae).

127. Stigmatomyces crassicollis Thaxt., Proc. Am. Acad. Arts Sci. 52: 661 (1917)

Leptocera caenosa (Rondani, 1880) (Diptera, Sphaeroceridae) Be

Leptocera fontinalis (Fallén, 1826) Be

Leptocera lutosoidea (Duda, 1938) Be

Opacifrons humida (Haliday, 1836) (Diptera, Sphaeroceridae) Be

Spelobia rufilabris (Stenhammar, 1855) (Diptera, Sphaeroceridae) Be

Sphaeroceridae sp. indet. (Diptera) Be

128. Stigmatomyces divergatus Thaxt., Mem. Am. Acad. Arts Sci. 16: 122 (1931)

Apteromyia claviventris (Strobl, 1909) (Diptera, Sphaeroceridae) Be

Spelobia parapusio (Dahl, 1909) (Diptera, Sphaeroceridae) Be

Spelobia sp. Be

129. Stigmatomyces entomophilus (Peck) Thaxt., Proc. Am. Acad. Arts Sci. 36: 398 (1900) [1901]

Drosophila funebris (Fabricius, 1787) (Diptera, Drosophilidae) Nl

130. Stigmatomyces hydrelliae Thaxt., Proc. Am. Acad. Arts Sci. 36: 404 (1900) [1901]

Hydrellia albilabris (Meigen, 1830) (Diptera, Ephydridae) Nla

a New record: Noord-Brabant Province, Udenhout, nature reserve De Brand, 51.631777N 5.132998E, 14–21 Jun. 1990, leg. Working Group Insects of the Royal Dutch Natural History Association (KNNV), malaise trap (van Zuijlen et al. 1996), on Hydrellia albilabris (Meigen, 1830) (Diptera, Ephydridae), slide WR1746 (will be deposited at FI, Herbarium Universitatis Florentinae, Florence, Italy), det. W. Rossi, comm. J.W.A. van Zuijlen.

131. Stigmatomyces limosinae Thaxt., Proc. Am. Acad. Arts Sci. 36: 406 (1900) [1901]

Spelobia clunipes (Meigen, 1830) (Diptera, Sphaeroceridae) Be

Spelobia talparum (Richards, 1927) Nl

132. Stigmatomyces majewskii H.L. Dainat, Manier & Balazuc, Bull. Trimest. Soc. Mycol. Fr. 90: 171 (1974)

Drosophila subobscura Collin, 1936 (Diptera, Drosophilidae) Nl

133. Stigmatomyces minilimosinae T. Majewski, Polish Bot. Stud. 1: 122 (1990)

Minilimosina parvula (Stenhammar, 1855) (Diptera, Sphaeroceridae) Be

134. Stigmatomyces platensis Speg., Anal. Mus. Nac. Hist. Nat. B. Aires 29: 676 (1917)

Paralimosina fucata (Rondani, 1880) (Diptera, Sphaeroceridae) Be

Paralimosina subcribrata (Rohacek, 1977) Be

135. Symplectromyces vulgaris (Thaxt.) Thaxt., Mem. Am. Acad. Arts Sci. 13: 315 (1908)

Philonthus sp. (Coleoptera, Staphylinidae) Be

Quedius curtipennis Bernhauer, 1908 (Coleoptera, Staphylinidae) Be

Quedius fuliginosus (Gravenhorst, 1802) Be

Quedius fumatus (Stephens, 1833) Be

Quedius lateralis (Gravenhorst, 1802) Nl

Quedius levicollis (Brullé, 1832) Bea

Quedius maurorufus (Gravenhorst, 1806) Nl

Quedius mesomelinus (Marsham, 1802) Be, Nl

Quedius sp. Be

a Host as Quedius tristis (Gravenhorst, 1802) in De Kesel et al. (2020).

136. Teratomyces actobii Thaxt. Proc. Am. Acad. Arts Sci. 29: 98 (1894)

Gabrius nigritulus (Gravenhorst, 1802) (Coleoptera, Staphylinidae) Be

Gabrius sp. Be

137. Teratomyces philonthi Thaxt., Proc. Am. Acad. Arts Sci. 35: 432 (1901)

Gabrius nigritulus (Gravenhorst, 1802) (Coleoptera, Staphylinidae) Be

Gabrius trossulus (Nordmann, 1837) Nla

Gabrius sp. Be

Quedius nitipennis (Stephens, 1833) (Coleoptera, Staphylinidae) Be

Quedius sp. Be

a Host as Philonthus trossulus Nordmann, 1837 in Middelhoek (1943a).

138. Troglomyces manfrediae S. Colla [as ‘manfredii’], Nuovo G. Bot. Ital. 39: 451 (1932)

Julida sp. indet. Be

139. Troglomyces triandrus Santam. & Enghoff, Organ. Divers. Evol. 15: 253 (2015)

Archiboreoiulus pallidus (Brade-Birks, 1920) (Julida, Blaniulidae) Be

140. Zodiomyces vorticellarius Thaxt., Proc. Am. Acad. Arts Sci. 25: 263 (1891)

Helochares punctatus (Sharp, 1869) (Coleoptera, Hydrophilidae) Nl

Helochares sp. Be

Doubtful records and combinations

Laboulbenia elegans Thaxt. on Harpalus affinis (Schrank, 1781) (Coleoptera, Carabidae) [as Harpalus aeneus (Fabricius, 1775)] (Middelhoek 1949). This material could not be verified since the Middelhoek collection is currently untraceable, but it likely represents L. coneglianensis. Laboulbenia coneglianensis is reported from species of Harpalus Latreille, 1802 and Ophonus Dejean, 1821 in Europe, whereas L. elegans is thus far only confirmed from New England, USA (Thaxter 1890, 1896).

Laboulbenia flagellata [as Laboulbenia elongata Thaxt.] on Calathus erratus (Sahlberg, 1827) (Coleoptera, Carabidae) (Middelhoek 1947b). The material is incomplete and impossible to verify. Given the host, it is doubtful that this report represents L. flagellata. Possibly it is L. calathi T. Majewski, which is already known from the Netherlands (Haelewaters et al. 2012b).

Laboulbenia flagellata on Pterostichus nigrita (Paykull, 1790) (Coleoptera, Carabidae) (Meijer 1975). This record possibly represents L. pseudomasei Thaxt. but we cannot verify because the material of Meijer is untraceable. Pterostichus nigrita is routinely reported as host to L. pseudomasei, not L. flagellata (Thaxter 1899; Scheloske 1969; Majewski 1994; Santamaría 1998; De Kesel et al. 2020). Both species are easily distinguished with morphological characters.

Laboulbenia pedicellata on Trechus quadristriatus (Schrank, 1781) (Coleoptera, Carabidae) (Meijer 1975). This would be the only worldwide record of L. pedicellata on a species of Trechus Clairville, 1806 and thus is likely incorrect. Laboulbenia pedicellata is generally reported on species of Bembidion Latreille, 1802 sensu lato (Coleoptera, Carabidae) and Dyschirius Bonelli, 1810 (Coleoptera, Carabidae) (Haelewaters et al. 2019a).

Discussion

New species and new records

In this paper, we describe two new species of Laboulbeniales based on the combination of molecular data, morphology, and ecology (host association). These are Hesperomyces halyziae on Halyzia sedecimguttata in Belgium and the Netherlands, and Laboulbenia quarantenae on Bembidion biguttatum in Belgium. Additionally, Laboulbenia aubryi and Rhachomyces spinosus are newly reported from Belgium. Seven previously described species of Laboulbeniales are reported for the first time from the Netherlands: Chitonomyces melanurus, Euphoriomyces agathidii, Laboulbenia fasciculata, Laboulbenia metableti, Laboulbenia pseudomasei, Rhachomyces canariensis, and Stigmatomyces hydrelliae.

The report of L. aubryi from Belgium is only the third one from Europe. Laboulbenia aubryi was thus far only recorded from India, Nepal, Poland, and Spain (type). Reported hosts are species in Amara Bonelli, 1810 (= Bradytus Stephens, 1827, = Leironotus Ganglbauer, 1892) (Santamaría et al. 1991; Santamaría 1998; Majewski 1999), a diverse genus that is only exceptionally reported with Laboulbeniales (Santamaría et al. 1991). Scheloske (1969) mentioned L. flagellata on Amara plebeja (Gyllenhal, 1810), but considered it an accidental host (“Zufallswirt”). Moreover, based on its simple outer appendage, L. aubryi can easily be separated from L. flagellata. The closest related species, morphologically speaking, is L. argutoris Cépède & F. Picard, but L. aubryi can be separated from it by the insertion cell that is free from the perithecium wall and by the structure of its inner appendage (Santamaría 1998).

Rhachomyces spinosus was recently described from Spain (Santamaría et al. 2020). The most characteristic feature of this species is the spinous process on the second cell of the primary appendage, absent in similar species R. lavagnei (F. Picard) W. Rossi and R. sciakyi W. Rossi. The reported host for R. spinosus in both Belgium and Spain is Syntomus foveatus (Coleoptera, Carabidae). Rhachomyces lavagnei is found on Microlestes spp. and R. sciakyi on Pseudomesolestes sp. All these hosts are placed in the subtribe Dromiusina (Harpalinae, Lebiini); it is possible that these species of Rhachomyces have a high degree of host specificity, which will only come to light as more material will be collected.

Chitonomyces melanurus is easily recognized from other congeneric species by the apically hooked, dark brown to blackish basal cell of its primary appendage. Nine species of Chitonomyces Peyr. occur in Europe, all of them occupying a specific position of the host integument. Chitonomyces melanurus grows almost exclusively on the upper margin of the left elytron of Laccophilus Leach, 1815 water beetles (Coleoptera, Dytiscidae). It has thus far has been reported in Europe from Austria (type), Belgium, Croatia, Finland, France, Germany, Hungary, Italy, Poland, Spain, Ukraine, United Kingdom; also found in Asia and Africa (Bánhegyi 1960; Huldén 1983; Santamaría et al. 1991; Majewski 1994; De Kesel and Werbrouck 2008; Rossi 2018).

The Dutch report of E. agathidii is found on Agathidium laevigatum, the host species from which the type was described (Maire 1920). Euphoriomyces agathidii is thus far found on members of Agathidium Panzer, 1796, Amphicyllis Erichson, 1845, and Cyrtusa Erichson, 1842 (Coleoptera, Leiodidae) in Bulgaria, Germany, Italy, Morocco (type), Poland, South Korea, Spain, and Sweden (Huldén 1983; Majewski 1994; Lee et al. 2007; Rossi et al. 2018). Our material is consistent with E. agathidii, with two mature perithecia at one side and a third, immature perithecium at the other side of the receptacular axis.

Laboulbenia fasciculata is recognized by the receptacular cell V, which proliferates upwards in a series of 4–8 superposed cells V’ gradually decreasing in size. Each of these cells V’ gives rise to a small trapezoidal cell that carries an appendage consisting of cells separated by dark and constricted septa. This species is very widespread, with reports across Europe, in Africa, Asia, and North and South America. Hosts are members of Carabidae, often Chlaenius Bonelli, 1810 (subfamily Harpalinae) and Patrobus Dejean, 1821 (subfamily Trechinae), but also several other genera in subfamilies Cicindelinae, Brachininae, Harpalinae, Nebriinae, Omophroninae, Patrobinae, and Trechinae (Santamaría et al. 1991). The reports on Omophron spp. are sometimes considered a form of L. fasciculata but this is not accepted by all (Spegazzini 1914; Majewski 1994; but Santamaría 1998).

The status of L. metableti as a separate species has been disputed. Formally synonymized with L. notiophili by Rossi and Santamaría (2006), De Kesel et al. (2020) reinstated L. metableti as a separate species based on characteristics of the appendage system. This species has a European distribution, with reports in Andorra, Austria, Belgium, Finland, Germany (type), Hungary, Italy, Poland, Russia, and the United Kingdom (reviewed in Rossi and Santamaría 2006). Hosts are species of Syntomus Hope, 1838 (= Metabletus Schmidt-Goebel, 1846) (Coleoptera, Carabidae, Harpalinae, Lebiini). We propose using molecular characters to resolve the debate given the taxonomic confusion of species of Laboulbenia on European hosts in the Lebiini tribe: L. baetica Balazuc, L. blanchardii Cépède, L. cymindicola Speg., L. metableti, L. notiophili, and L. pulchella Speg.

Laboulbenia pseudomasei is recognized by cell V that has an internal convex margin and is separated from the perithecium (Villarreal et al. 2010). Cell V sometimes proliferates into a simple or divided branch that grows upwards between the perithecium and insertion cell (Majewski 1994; Santamaría 1998). Rossi and Weir (1997) illustrated that L. pseudomasei can be morphologically highly variable even on a single host insect. Also in the newly reported material from the Netherlands, L. pseudomasei was variable, with the thallus from the right elytron without proliferation of cell V, and the thallus from the prosternum with proliferation of cell V. The geographic distribution of L. pseudomasei is problematic; many old records are unillustrated and the specimens are not preserved (Rossi and Weir 1997).

Rhachomyces canariensis was described from Tenerife (Thaxter 1900) and has since been reported from several countries in Europe and North Africa, Madeira, and the Canary Islands, always associated with species of Trechus Clairville, 1806 (Coleoptera, Carabidae) (Arndt and Santamaría 2004). Majewski (1994) noted the variability of this species and Tavares (1985) suggested material from large geographic distances to the type locality be segregated into a separate taxon.

The only species of Laboulbeniales found on Hydrellia Robineau-Desvoidy, 1830 flies (Diptera, Ephydridae) is S. hydrelliae. Thaxter (1901) described it from Kittery Point in Maine, USA (Thaxter 1901) and it has since then been reported in Finland, France, Italy, Poland, Portugal, Russia, the United Kingdom (Santamaría and Rossi 1993, Weir and Rossi 1995), and New Zealand (Hughes et al. 2004). The new report from the Netherlands is the first one on the European continent in 25 years. Stigmatomyces hydrelliae is recognized by its straight appendage with sterile basal cell and stout antheridia, the spiralled cell walls of the perithecium, and the rounded perithecial apex with one of the lip cells forming a slender, bluntly pointed projection. Hughes et al. (2004) noted that S. hydrelliae thalli from New Zealand are different in their perithecial wall cells not being spiralled and lacking apical projections at the perithecial apex.

Checklist

The current list of thallus-forming Laboulbeniomycetes from Belgium and the Netherlands includes 140 species. Sixty-three species have been found in both countries. A total of 118 species are found in Belgium, and 85 species in the Netherlands. Of the 140 species in the checklist, 55 have not (yet) been reported from the Netherlands, and 22 species have not (yet) been reported from Belgium. Laboulbeniales research in both Belgium and the Netherlands has also resulted in the discovery of new taxa; over the years, 16 species have been described based on material from Belgium and/or the Netherlands (Table 3). It is remarkable that we keep finding undescribed species in two of the most urbanized countries in the world. The reason for this can be found in the fact that Laboulbeniomycetes are severely understudied; only a handful of researchers work on these fungi. In addition, some of the most recently described species are the result of previously unavailable molecular data, long-term study of humid habitats, and focus on unexplored niches.

Table 3.

Species of Laboulbeniales described based on type material from Belgium (Be) and the Netherlands (Nl).

Country Laboulbeniales species Host species Host classification Reference
Nl Asaphomyces tubanticus [as Barbariella tubantica] Catops nigricans Coleoptera, Leiodidae Middelhoek (1949)
Nl Cantharomyces elongatus Syntomium aeneum Coleoptera, Staphylinidae Haelewaters and De Kesel (2013)
Nl Bordea denotata Bibloporus bicolor Coleoptera, Staphylinidae Haelewaters et al. (2014)
Be Cryptandromyces euplecti Euplectus sanguineus Coleoptera, Staphylinidae Santamaría (2001)
Be, NL Diphymyces kaaistoepi Choleva cisteloides, C. fagniezi Coleoptera, Leiodidae De Kesel and Haelewaters (2019)
Be, NL Hesperomyces halyziae Halyzia sedecimguttata Coleoptera, Coccinellidae This paper
Nl Laboulbenia barbara Philonthus punctus Coleoptera, Staphylinidae Middelhoek (1943a)
Be Laboulbenia quarantenae Bembidion biguttatum Coleoptera, Carabidae This paper
Be Laboulbenia elaphri Elaphrus cupreus Coleoptera, Carabidae Spegazzini (1915)
Be Laboulbenia hyalopoda Paradromius linearis Coleoptera, Carabidae De Kesel (1998)
Be, NL Laboulbenia littoralis Cafius xantholoma Coleoptera, Staphylinidae De Kesel and Haelewaters (2014)
Nl Mimeomyces zeelandicus Heterothops binotatus Coleoptera, Staphylinidae Middelhoek (1943a)
Be Peyritschiella heinemanniana Xantholinus longiventris Coleoptera, Staphylinidae De Kesel (1999)
Be Phaulomyces simplocariae Simplocaria semistriata Coleoptera, Byrrhidae De Kesel (1994)
Be, NL Rickia laboulbenioides Cylindroiulus latestriatus Julida, Julidae De Kesel et al. (2013)
Be Troglomyces triandrus Archiboreoiulus pallidus Julida, Blaniulidae Enghoff and Santamaría (2015)

This checklist is based on fungal records obtained from at least 283 host species (including only those identified to species level). To increase the number of thallus-forming Laboulbeniomycetes known from Belgium and the Netherlands, future research should focus on screening Acari (with Rickia), Blattodea (Herpomyces–especially in the Netherlands), Coleoptera (many genera), Corixidae (Coreomyces), Diplopoda (Diplopodomyces, Troglomyces), Diptera (Stigmatomyces), Hebridae (Tavaresiella, Triceromyces), and Mallophaga (Trenomyces). Within Coleoptera, the beetles, aquatic and semi-aquatic hosts, such as Dytiscidae (Chitonomyces), Hydraenidae (Autoicomyces, Hydrophilomyces, Thripomyces), and Hydrophilidae (Chaetarthriomyces, Eusynaptomyces) deserve special attention. More genera of Laboulbeniales that are currently not yet recorded from either Belgium or the Netherlands, could be discovered on Anthicidae (Dioicomyces), Ptiliidae (Siemaszkoa), Silvanidae (Cucujomyces), Staphylinidae (Amorphomyces, Diplomyces, Dipodomyces, Haplomyces, Mimeomyces, Sphaleromyces), and Tenebrionidae (Dimeromyces).

As Laboulbeniomycetes research progresses, lesser known host groups will need to be incorporated into our studies. This will eventually require intensified collaborations with specialist entomologists, as well as screening museum insect collections and the use of different collecting methods. That different sampling techniques have an impact on Laboulbeniales studies may be illustrated by our work with Rickia wasmannii Cavara. Based on pitfall trapping, Haelewaters et al. (2015a) reported R. wasmannii from three host species: Myrmica sabuleti Meinert, 1861 (parasite prevalence 38%), M. scabrinodis Nylander, 1846 (11%), and M. ruginodis Nylander, 1846 (0.55%). Direct sampling from a M. scabrinodis nest at the same locality in the Netherlands, however, resulted in a 100% prevalence (De Kesel et al. 2016).

Finally, undersampled habitats have been cited repeatedly as one of the main sources to find undescribed fungi (e.g., Blackwell 2011, Hawksworth and Lücking 2017, Wijayawardene et al. 2020). This is especially true for the Laboulbeniomycetes. Sampling from dung, fresh and brackish water, animal nests, caves, carcasses, and rotting plant debris has greatly contributed to discoveries in this field of research, not only adding to numbers of described species but also building on our understanding of the ecology of these minute fungi. For example, Pfliegler et al. (2016) sampled ants and their associates from ant nests and, for the first time since its description (Cavara 1899), R. wasmannii was observed on hosts other than Myrmica, including inquiline mites and a fly larva. A survey of Laboulbeniales from coprophilic beetles on Galloway dung in Belgium resulted in two reports of species that until then had only been found in Poland, thus representing a large geographical range expansion (De Kesel 2010). And signal crayfish traps in nature reserve ‘De Kaaistoep’ have thus far revealed an undescribed species of Diphymyces (De Kesel and Haelewaters 2019) and more material is awaiting detailed study.

Key to Laboulbeniomycetes from Belgium and the Netherlands

1 Dioecious; on Blattodea (cockroaches) 50 (Herpomyces)
Thalli mostly monoecious; on other host groups 2
2 Perithecial wall cells numerous, subequal, always ≥ 6 cells per vertical row 3
Perithecial wall with < 6 cells per vertical row 7
3 Receptacle uniseriate, composed of numerous superposed cells 5
Receptacle multiseriate, often massive 4
4 Receptacle turbinate, with apical depression holding numerous sterile appendages, stalked perithecia and antheridial branchlets; on Hydrophilidae Zodiomyces vorticellarius
Receptacle not turbinate, bearing numerous perithecia and appendages laterally; on Carabidae and Staphylinidae Euzodiomyces lathrobii
5 Perithecium with an apical, darkened rostrum; receptacle with 4–5 cells; on Ptiliidae Kainomyces rehmanii
Perithecium without a rostrum; receptacle with > 5 cells 6
6 Perithecium long-necked, without lobes or fine appendages on the perithecial wall; on Hydrophilidae Rhynchophoromyces anacaenae
Perithecium without long neck, ostiolum with 4 fine ligulae, lower wall bearing slender ramified appendices; on Dryopidae Helodiomyces elegans
7 Antheridia simple, flask shaped; release of spermatia through small necks 8
Antheridia grouped into a compound structure with wall 44
8 Sterile appendages unicellular with black basal septum; antheridia small, always with black basal septum; receptacle formed by 3 vertical tiers of cells (not always clear), at least one tier partly or entirely flanking the perithecium 52 (Rickia)
Not this combination 9
9 Suprabasal cell of the receptacle (cell II) produces multi-celled secondary appendages; the latter supporting a perithecium (with cell VI) at their base Compsomyces lestevae
Cell II not producing secondary appendages 10
10 Perithecial wall with an elongated accessory cell along its outer venter; unicellular outgrowths are formed above the foot; on Cercyon (Hydrophilidae) 11
Perithecium without accessory cell; no such outgrowths above the foot 12
11 Lower receptacular cells isodiametric; perithecium neck more or les straight Hydrophilomyces cf. gracilis
Lower receptacular cells flattened; perithecium neck strongly curved Hydrophilomyces cf. hamatus
12 Cell VII and basal cells of the perithecium clearly visible in mature perithecia 13
Cell VII and basal cells of the perithecium not visible in mature perithecia 40
13 Receptacle produces longitudinal septa, leading to a suprabasal complex with numerous secondary appendices 14
Receptacle stays a series of superposed cells, rarely forming longitudinal septa, not forming a suprabasal complex or secondary appendices 20
14 Receptacle composed of a series of superposed cells (4–5 or more), each forming on one side a basal cell with numerous, fairly large, pigmented and multicellular appendages; thalli usually with only one perithecium 56 (Rhachomyces)
Not with these features 15
15 Thallus hyaline; appendages not in bunches; On Cholevinae (Leiodidae) Asaphomyces tubanticus
Thallus moderately to deeply pigmented in some parts; appendages appear in bunches on the receptacle 16
16 Receptacle asymmetrical 17
Receptacle mostly symmetrical 18
17 Antheridia in lateral series on fertile appendages; dorsal and ventral cell of the triangular receptacle supporting a series of appendages and their basal cells; perithecium stalked by elongated cells VI and VII Idiomyces peyritschii
Antheridia never organized in lateral series; appendages not in series; receptacle 5-celled; cells VI and VII relatively short 62 (Laboulbenia)
18 Appendages with pointed-curved tips, darkened septa; antheridia terminal, flask shaped, not forming ramifications with age 19 (Teratomyces)
Appendages with rounded tips, with series of intercalary antheridia, the latter ramifying into new appendages with age Symplectromyces vulgaris
19 Cells I and II from receptacle becoming brown with age; basal cells of appendages with laterally aligned antheridia/septa Teratomyces philonthi
Cell I hyaline, contrasting with a deep blackened cell II; basal cells of appendages without such laterally aligned septa Teratomyces actobii
20 Primary appendage bicellular, both cells separated by a dark constricted septum; antheridium below the primary appendage; on aquatic Coleoptera 21
Primary appendage more developed 22
21 All 4 vertical tiers of the perithecial wall have 4 cells each 109 (Chitonomyces)
Only 2 vertical tiers of the perithecial wall have 4 cells, the others have 6 cells; on Haliplidae Hydraeomyces halipli
22 Receptacle composed of ≥ 4 cells 23
Receptacle composed of ≤ 3 cells 26
23 Primary receptacle composed of a chain of cells (≥ 3) 24
Primary receptacle composed of cells I and II, entire receptacle with five cells 62 (Laboulbenia)
24 Perithecium with obtuse apex and inconspicuous neck Misgomyces dyschirii
Perithecium with long neck and differentiated venter 25
25 Antheridia sessile, develop as corner cells of the primary appendage; Receptacle cells flattened, broadening upwards Ecteinomyces trichopterophilus
Antheridia not sessile but formed on lateral branchlets; receptacle cells elongate Botryandromyces heteroceri
26 Cell III flattened and entirely appressed against the perithecium; on Julida 113 (Troglomyces)
Cell III different; on Hexapoda 27
27 On Coleoptera 29
Not on Coleoptera 28
28 Basal cell of appendage dark; perithecial apex with outgrowths; on Forficula (Dermaptera, Forficulidae) Distolomyces forficulae
On Diptera 114 (Fanniomyces & Stigmatomyces)
29 Primary appendage easily breaking off at its strongly narrowed basal cell; on Kateretidae Aphanandromyces audisioi
Primary appendage persistent 30
30 Receptacle cells (I, II, III) more or less superposed 31
Receptacle cells not superposed (cell I and III touching) 39
31 Distal cell of primary appendage is a simple antheridium, with efferent neck and spine Bordea denotata
Primary appendage without such a single and terminal antheridium 32
32 Antheridial structures are born on corner cells of appendage axis cells 33
Antheridial branches not born from corner cells 36
33 Basal (m, n, n’) and stalk cells (VI, VII) of the perithecium small (together < 25 µm long); on Hydrophilidae Chaetarthriomyces crassiappendicatus
Basal (m, n, n’) and stalk cells (VI, VII) ≥ 25 µm long; on Staphylinidae 34
34 Cell III mostly without antheridial branches, with or without perithecium; cells VI and VII of similar length Stichomyces conosomatis
Cell III always with antheridial branches, never with perithecium; cell VI much taller than cell VII 35
35 Thallus forms perithecia and corner cells on one side (anterior) Rhadinomyces pallidus
Thallus forms perithecia and corner cells on both sides (anterior and posterior) Rhadinomyces cristatus
36 Primary appendage simple, composed of numerous similar superposed cells 124 (Cryptandromyces)
Primary appendage branched 37
37 Cell VI adnate to cell II; exclusively on Cholevinae (Leiodidae) Diphymyces kaaistoepi
Cell VI supported by cell II; mostly on Staphylinidae, rarely on Cholevinae (Leiodidae) 38
38 Cell I tall and elongated, cell II flattened Mimeomyces zeelandicus
Cell I very short, cell II not flattened (isodiametric) 126 (Corethromyces)
39 Perithecial tip with prominent ostiolar lips and lobes; appendage short, with sessile lateral antheridia on each cell; fresh thalli often greenish-yellow; on Coccinellidae 127 (Hesperomyces)
Perithecial tip without such lobes; appendage long, with lateral antheridia on few cells; not on Coccinellidae 124 (Cryptandromyces)
40 Receptacle between foot and cell VI with ≥ 3 cells. 41
Receptacle between foot and cell VI with 2 cells; foot entirely black Phaulomyces simplocariae
41 Receptacle a series of superposed cells, many of which laterally producing perithecia and/or appendages Euphoriomyces agathidii
Receptacle a series of superposed cells without lateral cells bearing perithecia and appendages 42
42 Receptacle with flattened and finely appendiculate cells above cell III; Foot entirely black; on Corixidae (Hemiptera) Coreomyces arcuatus
Receptacle without such flattened cells above cell III; foot with a small blackish dot; on Ptiliidae 43
43 The appendage is a prolongation of the receptacle axis, the perithecium is lateral Siemaszkoa ptenidii
The perithecium is often terminal and in continuation with the receptacular axis Siemaszkoa fennica
44 Cell I laterally extending and supporting a series of cells derived from cell II; thallus dioecious Dimorphomyces myrmedoniae
Cell I not laterally extending; thallus monoecious 45
45 Primary receptacle composed of a chain of ≥ 3 cells Misgomyces dyschirii
Primary receptacle not a chain of cells 46
46 Primary appendage fertile, with a compound antheridium 47
Primary appendage sterile or absent 49
47 Compound antheridium with efferent neck and tall cell on the outer side; on Carabidae Eucantharomyces stammeri
Compound antheridium different, never with efferent neck; on Staphylinidae and Dryopidae (= Parnidae) 48
48 Primary appendage is entirely transformed into a compound antheridium, with spine Haplomyces texanus
Compound antheridium is an intercalary structure of the primary appendage 129 (Cantharomyces)
49 Receptacle formed by 3 horizontal tiers of cells; antheridia compound, sessile, often on the median series; sterile appendages unicellular 134 (Peyritschiella)
Receptacle differently organized; sterile appendages multicellular; antheridial structure stalked, large 140 (Monoicomyces)
50 Secondary receptacle (female thallus) without concentrically organized cells Herpomyces ectobiae
Secondary receptacle a series of concentrically organized and flattened cells 51
51 Secondary receptacle ≤ 80 µm long, with rounded apex and partially darkened cells Herpomyces stylopygae
Secondary receptacle ≥ 100 µm long, with pointed apex and without dark pigmentations Herpomyces periplanetae
52 Perithecium almost entirely embedded in the receptacle Rickia peyerimhoffii
Anterior part of the perithecium free 53
53 On Diplopoda 54
On other arthropods 55
54 Dorsal margin of the perithecium free in its upper third; anterior series of receptacle consisting of 2(–3) cells Rickia laboulbenioides
Dorsal margin of the perithecium only free at the apex; Anterior series of receptacle consisting of > 2 cells Rickia dendroiuli
55 Cell I 12–18 µm long; on Staphylinidae Rickia proteini
Cell I 60–90 µm long; on Myrmica (Hymenoptera, Formicidae) Rickia wasmannii
56 Primary appendage hyaline, 3-celled, different from other appendages; On Syntomus (Carabidae) Rhachomyces spinosus
Primary appendage pigmented, identical to secondary appendages 57
57 Receptaculum between cells I and VI usually with < 6 cells, sterile appendages very long; on Lathrobium (Staphylinidae) Rhachomyces pilosellus
Receptaculum between cells I and VI composed of ≥ 6 cells; sterile appendages do not exceed perithecial apex 58
58 Cells of the B-appendages of unequal length 59
Cells of the B-appendages of similar to equal length 60
59 B-appendages elongate, slender, tapering upwards; On Philonthus (Staphylinidae) Rhachomyces philonthinus
B-appendages short, stout, width broad rounded apex; On Thalassophilus (Carabidae) Rhachomyces tenenbaumii
60 Cell VI elongate and situated in the median to subapical part of the (secondary) receptacle; On Othius (Staphylinidae) Rhachomyces furcatus
Cell VI short, distally on the (secondary) receptacle; on Carabidae 61
61 Perithecial apex with black spots; terminal cell of the B-appendages widest in the middle; on Acupalpus (Carabidae) Rhachomyces lasiophorus
Perithecial apex hyaline; terminal cell of B-appendages cylindrical, usually proliferating; on Trechus (Carabidae) Rhachomyces canariensis
62 Insertion cell absent 63
Insertion cell present 65
63 Appendages with large basal cells and dark septa; on Carabidae Laboulbenia fasciculata
Appendages filiform, with fine basal cells and dark septal on Gyrinidae 64
64 Perithecium with two hyaline apical outgrowths, one straight one hooked Laboulbenia gyrinicola
Both perithecial outgrowths with black spots, irregularly shaped Laboulbenia fennica
65 On Carabidae 66
On Staphylinidae 103
66 Insertion cell free 67
Insertion cell attached to the posterior margin of the perithecium (not free) 72
67 Foot almost hyaline with only a small black dot Laboulbenia hyalopoda
Foot entirely black 68
68 Cell V as tall as cell IV Laboulbenia clivinalis
Cell V smaller than cell IV 69
69 Outer appendage not branched 70
Outer appendage branched Laboulbenia pseudomasei
70 Inner appendage hardly branched, with a single antheridium Laboulbenia lecoareri
Inner appendage branched, with multiple antheridia 71
71 Lower 4–5 cells of outer appendage deeply pigmented in their middle; ostiolar papillae not conspicuous; on Syntomus (Carabidae) Laboulbenia metableti
Lower 4–5 cells of outer appendage evenly pigmented; ostiolar papillae conspicuous; on Amara (Carabidae) Laboulbenia aubryi
72 Cell V as tall as cell IV, or almost so 73
Cell V smaller than cell IV 78
73 Outer wall of perithecium with knobs Laboulbenia egens
Outer wall of the perithecium without knobs 74
74 Outer appendage without dark septum, growing beyond the perithecium Laboulbenia ophoni
Outer appendage with at least one dark septum, not growing beyond the perithecium 75
75 Cells IV and V flattened, broader than long; On Cillenus (Carabidae) Laboulbenia lichtensteinii
Cells IV and V isodiametric or longer than broad 76
76 Thallus and receptaculum poorly pigmented (yellow-amber); basal cell of outer appendage inflated; on Pogonus (Staphylinidae) Laboulbenia slackensis
Thallus and receptaculum strongly pigmented; basal cell of outer appendage not so inflated 77
77 Cell III flattened and oblique; posterior margin of cell IV longer than the one from cell III; insertion cell extremely flat and opaque Laboulbenia luxurians
Cell III not flattened; posterior margin of cell IV equal or shorter than the one from cell III; insertion cell well-formed and black Laboulbenia pedicellata
78 Outer appendage not growing beyond the perithecium Laboulbenia murmanica
Outer appendage growing beyond the perithecium 79
79 Outer appendage branched 80
Outer appendage not branched 90
80 Cell IV very long, often with a conspicuous dorso-apical bump, sometimes divided 81
Cell IV not so long, never divided, without dorso-apical bump 82
81 Outer appendage with > 2 branches; on Stenolophus (Carabidae) Laboulbenia anoplogenii
Outer appendage consisting of 2 branches; on Acupalpus (Carabidae) Laboulbenia acupalpi
82 Insertion cell on or above the middle of the perithecium; inner appendage less developed than outer appendage 83
Insertion cell below the middle of the perithecium 84
83 Thallus and receptaculum pale; septa from basal cells of outer appendage not darkened; on Paranchus albipes (Carabidae) Laboulbenia collae
Thallus and receptaculum strongly pigmented; septa from basal cells of outer appendage darkened Laboulbenia vulgaris
84 Outer side of the base of outer appendage strongly darkened 85
Outer side of the base of outer appendage not or only very slightly darkened 87
85 Thallus pale brown; appendages numerous, with tapering and pointed apices; on Dicheirotrichus (Carabidae) Laboulbenia giardii
Thallus deep brown; appendages not so numerous, not tapering, with rounded apices 86
86 Septum II/III clearly shorter than septum II/VI; cell V clearer than surrounding structures; on Harpalus and Ophonus (Carabidae) Laboulbenia coneglianensis
Septum II/III nearly as long as septum II/VI; cell V not much paler than surrounding structures; on Brachinus (Carabidae) Laboulbenia rougetii
87 Thallus often bent, anterior side of the thallus concave 89
Thallus not so bent, anterior side of the thallus fairly straight 88
88 Insertion cell near the base of the perithecium; outer appendage often composed of 4–6(–8) branches, resulting from successive dichotomies starting at the suprabasal cell Laboulbenia quarantenae
Insertion cell not so deep; outer appendage branched once or twice, not as dichotomies Laboulbenia flagellata sensu lato
89 Cell V quite small, less than half the length of cell IV; perithecium very slender, subcylindrical (not a stable feature); on Harpalus (Carabidae) Laboulbenia coneglianensis
Cell V longer, usually more than half the length of cell IV; perithecium more ovate; on Elaphrus (Carabidae) Laboulbenia elaphri
90 Insertion cell located at or above the middle of the perithecium; adaxial side of the perithecium half free 91
Insertion cell located well below the middle of the perithecium; adaxial side of the perithecium more than half free 95
91 Basal cells of outer appendage with darkened septa 93
Basal cells of outer appendage with normal septa 92
92 Cell VI broader than long Laboulbenia benjaminii
Cell VI longer than broad Laboulbenia argutoris
93 Basal cell of outer appendage inflated; inner appendage growing beyond the perithecium Laboulbenia inflata
Basal cell of outer appendage normal; inner appendage never beyond perithecium 94
94 Inner appendage composed of a single antheridium supported by one basal cell; on Asaphidion (Carabidae) Laboulbenia thaxteri
Inner appendage with ≥ 2 cells each supporting one or more antheridia Laboulbenia vulgaris
95 Outer appendage rotated relative to the perithecium; on Pterostichus diligens (Carabidae) Laboulbenia kajanensis
Outer appendage not rotated 96
96 Inner appendage growing far beyond the perithecium 97
Inner appendage not or hardly beyond the perithecium 98
97 Cell V clearly paler than surrounding cells and perithecium (III, IV and VI) 98
Cell V not paler than its surrounding cells Laboulbenia leisti
98 Cell IV (and cell III) evenly and deeply pigmented 100
Cell IV (and cell III) hyaline or pigmented, their outer margins distinctly more pigmented than inner margins 99
99 Cell VI longer than broad; thallus ≥ 230 µm long; on Calathus (Carabidae) Laboulbenia calathi
Cell VI isodiametric; thallus smaller; on Demetrias, Notiophilus and Paradromius (Carabidae) Laboulbenia notiophili sensu lato
100 Inner appendage hardly branched, with a single antheridium; cell IV longer than broad Laboulbenia lecoareri
Inner appendage branched, with multiple antheridia; cell IV isodiametrical 101
101 Cell V minute; upper margin of cell IV 4–6× the width of cell V 102
Cell V larger; upper margin of cell IV only 1–2× the width of cell V Laboulbenia eubradycelli
102 Lower 4–5 cells of outer appendage deeply pigmented in their middle; lower 3–4 cells of both branches of the inner appendage each producing a short straight branch Laboulbenia metableti
Lower 4–5 cells of outer appendage evenly pigmented; inner appendage differently constructed Laboulbenia notiophili sensu lato
103 Cell V as long as cell IV, or almost so 106
Cell V smaller than cell IV 104
104 Insertion cell free from the perithecium; outer appendage branched Laboulbenia dubia
Insertion cell attached to the posterior margin of the perithecium (not free); outer appendage not branched 105
105 Outer appendage with dark septa between basal cells; insertion cell near the base of the perithecium Laboulbenia stilicicola
Outer appendage without dark septa at the basal cells; insertion cell near the middle of the perithecium Laboulbenia atlantica
106 Outer appendage with at least one dark septum at the basal and suprabasal cells 108
Outer appendage without dark septa at the basal cells 107
107 Outer appendage forming a tuft of branches, posterior margins of both its basal and suprabasal cell entirely darkened Laboulbenia barbara
Outer appendage simple or forked once; posterior margin of suprabasal cell of outer appendage with black remains of primary appendage Laboulbenia cristata
108 Cell II hyaline; one black septum above the basal cell of the outer appendage Laboulbenia littoralis
Anterior part of cell II pigmented black; black septa between all basal cells of inner and outer appendage Laboulbenia philonthi
109 Perithecium with conspicuous outgrowths (spikes, thorns) 110
Perithecium without outgrowths; receptacle with outgrowth 111
110 Perithecial outgrowth, arising from the apical-most wall cell Chitonomyces paradoxus
Perithecial outgrowth lateral, arising from sub-apical wall cell Chitonomyces aculeifer
111 Suprabasal cell of the receptacle (Ia) flattened Chitonomyces bidessarius
Suprabasal cell of the receptacle (Ia) isodiametric 112
112 Receptacular outgrowth hyaline, straight or arcuate Chitonomyces italicus
Receptacular outgrowth black, straight, with conspicuously hooked apex Chitonomyces melanurus
113 Primary appendage with 1 antheridium, always situated in the lowest cell Troglomyces manfrediae
Primary appendage with 3 antheridia situated in the third, fourth and fifth cell Troglomyces triandrus
114 Appendage branched 115
Appendage an unbranched axis 116
115 Basal cell of appendage small, pigmented; appendage cells normal Fanniomyces burdigalensis
Basal cell of appendage elongate, not pigmented; appendage cells elongated Fanniomyces ceratophorus
116 Cell VI shorter than cell III; appendage consisting isodiametric to elongated cells 117
Cells III and VI equally long; appendage with dark basal cell, consisting of flattened cells; on Sphaeroceridae (Diptera) 120
117 Venter of perithecium without protuberances 118
Venter of perithecium with protuberances; on Ephydridae (Diptera) Stigmatomyces hydrelliae
118 Appendage arcuated or sigmoid; perithecial neck shorter than the venter; on Musca (Diptera, Muscidae) Stigmatomyces baeri
Appendage not arcuated; perithecial neck longer than venter; on Drosophila (Diptera, Drosophilidae) 119
119 Perithecial neck as long as venter; appendage hyaline, its axis composed of 4 cells; On Drosophila subg. Sophophora (Diptera, Drosophilidae) Stigmatomyces majewskii
Perithecial neck 2× as long as venter; appendage brown, its axis composed of 6 cells; On Drosophila subg. Drosophila (Diptera, Drosophilidae) Stigmatomyces entomophilus
120 Venter of perithecium without protuberances 121
Venter of perithecium with protuberances 122
121 Perithecial basal cells elongated, longer than the appendage Stigmatomyces limosinae
Perithecial basal cells not elongated, never longer than the appendage Stigmatomyces crassicollis
122 Perithecial apex abruptly becoming conical; appendage not proliferating Stigmatomyces platensis
Perithecial apex gradually tapering; appendage proliferating distally 123
123 Perithecial venter with numerous knobs, below the neck and also downwards Stigmatomyces minilimosinae
Perithecial venter with 4 knobs, only below the neck Stigmatomyces divergatus
124 Basal cells of the primary appendage dark brown on the outer side Cryptandromyces euplecti
Primary appendage entirely hyaline 125
125 Cell I supporting cell II; thallus > 125 µm long Cryptandromyces elegans
Cell I supporting cells II and III; thallus < 100 µm long Cryptandromyces bibloplecti
126 Basal cell of the receptacle with a black upgrowth; on Rugilus (Staphylinidae) Corethromyces stilici
Basal cell of the receptacle normal, without a black upgrowth; on Choleva (Leiodidae) Corethromyces henrotii
127 Upper and lower lobes of perithecium of equal length, not exceeding perithecial tip Hesperomyces coccinelloides
Upper lobes long, exceeding the perithecial tip; lower lobes short 128
128 On Halyzia (Coleoptera, Coccinellidae) Hesperomyces halyziae
On Harmonia, Tytthaspis (Coleoptera, Coccinellidae) Hesperomyces virescens sensu lato
129 Cell II of receptacle blackened Cantharomyces denigratus
Cell II never black, at most brownish or with a black spot 130
130 Basal cell of primary appendage supporting a 300–415 µm long unbranched series of 7–11 elongate cells Cantharomyces elongatus
Primary appendage not so long 131
131 Primary appendage not ramified Cantharomyces italicus
Primary appendage with ramifications 132
132 Primary appendage ramified above the suprabasal cell; basal cell not spherical 133
Primary appendage ramified above the basal cell, the latter spherical Cantharomyces robustus
133 Antheridium small, not reaching the upper and lower septa of the basal cell of the appendage Cantharomyces platystethi
Antheridium larger, reaching the lower (and upper) septum of the basal cell of the appendage Cantharomyces orientalis
134 Sterile appendages blackish brown, without conspicuous black septa Peyritschiella heinemanniana
Sterile appendages hardly pigmented, with black septa 135
135 Lower horizontal tier of cells pigmented black, septa between cells obscured 136
Lower horizontal tier of cells not as pigmented, septa between cells visible 138
136 Distal part of receptacle broad; upper tier composed of > 20 cells Peyritschiella biformis
Upper tier of the receptacle with < 15 cells; lateral sides of median tier each produce one pigmented outgrowths (some reach the upper tier) 137
137 Thallus with 2 perithecia Peyritschiella furcifera
Thallus with (2–)3–12 perithecia Peyritschiella vulgata
138 Median cell of both lowest horizontal tiers as long as neighboring cells Peyritschiella protea
Median cell of both lowest horizontal tiers much larger than neighboring cells, the latter becoming smaller outwards. 139
139 Perithecium usually with auricula; Third and second horizontal tier of similar length Peyritschiella dubia
Perithecium without auricula; third horizontal tier longer than second Peyritschiella princeps
140 Secondary receptacula unicellular 141
Secondary receptacula multicellular 146
141 Secondary receptacula pigmented 145
Secondary receptacula hyaline 142
142 Cell VI much longer than perithecium Monoicomyces myllaenae
Cell VI shorter than perithecium 143
143 Perithecium asymmetrical and bent; antheridium usually without apical branchlets Monoicomyces matthiatis
Perithecium symmetrical, straight; antheridium with several apical branchlets 144
144 Basal cell of primary appendage at least partially pigmented, not narrowing towards the apex Monoicomyces homalotae
Basal cell of primary appendage entirely hyaline, narrowing towards the apex Monoicomyces britannicus
145 Antheridial and primary appendages very long, reaching beyond the perithecial apex Monoicomyces fragilis
Antheridial and primary appendages shorter, not reaching beyond the perithecial apex Monoicomyces nigrescens
146 Secondary receptaculum pigmented Monoicomyces bolitocharae
Secondary receptaculum hyaline 147
147 Secondary and antheridial appendages blackish brown Monoicomyces californicus
Secondary and antheridial appendages hyaline or hardly pigmented, never blackish brown Monoicomyces invisibilis

Acknowledgements

D. Haelewaters received funding from the Uyttenboogaart-Eliasen Foundation and through a SYNTHESYS+ grant (no. BE-TAF-151), financed by the Horizon 2020 Research Infrastructures Programme of the European Commission. We want to take the opportunity to recognize friends and collaborators for providing and/or identifying infected insects throughout the years: Mario Amalfi, Berend Aukema, Wim Baert, Michiel Boeken, Peter Boer, Johan Bogaert, Emiel H.M. Bouvy, André Braeckman, Silvano Canzoneri, Luc De Bruyn, Gerdien De Kock, Kris Decleer, Wouter Dekoninck, Albert J. Dees, Patrice Deramaix, Konjev Desender, Shanice De Weggheleire, Didier Drugmand, Marc Dufrène, Henrik Enghoff, Ron Felix, Cyrille Gerstmans, Guy Haeghebaert, Frederik Hanssens, Bart Horvers, Ivan Hoste, Sophie Janssens, Rudy Jocqué, Peter-Jan Keizer, Ilse Kranen, Mark Lammers, Violet Middelman, Jinze Noordijk, Theo M.J. Peeters, C. Lidwien Raak-van den Berg, Ivo Raemakers, Jindřich Roháček, Menno Schilthuizen, Edwin Schuller, Dieter Slos, Piet Stoffelen, Henk Spijkers, Tom Van den Neucker, Douwe van der Ploeg, Joke van Erkelens, Marck Van Kerckvoorde, Thierry Vercauteren, Paul S. van Wielink, Tom Werbrouck, Jan Willem A. van Zuijlen, Oscar Vorst, and Remco Vos. We should also acknowledge the Emergency Temporary Access Service developed by HathiTrust in response to the COVID-19 pandemic and subsequent lockdown, which made it possible for us to access necessary literature. Finally, we thank Alejandra Gutierrez, Patricia Kaishian, and Walter Rossi for reviewing the paper and providing valuable suggestions for improvement.

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