A preliminary world checklist of fern-mining insects.

Compared to the leaf-miners and stem-miners on flowering plants, the miners on ferns (including both Lycopodiophyta and Polypodiophyta in the broad sense) are less known. Knowledge of miners and their host plants is essential to fully understand plant-insect interactions. Although there are many scattered records on fern miners, a worldwide checklist has not been reported. We provide a preliminary checklist of fern-mining insects and their host plants worldwide. Altogether, we found records for 128 species and 18 families of fern miners, mainly that feed on Dennstaedtiaceae, Equisetaceae, Polypodiaceae and Aspleniaceae. Fern miners belonged to four orders: Diptera (51 species; 39.8%), Coleoptera (33 species; 25.8%), Lepidoptera (28 species; 21.9%) and Hymenoptera (16 species; 12.5%). They are primarily known from the Palaearctic Region, Nearctic Region, Neotropical Region and Oriental Region. Jie Yang, Xuexiong Wang, Kevin Jan Duffy, Xiaohua Dai.

Introduction

Leaf/stem miners are endophagous insects whose larvae feed on parenchyma or epidermal cells and form visually distinctive feeding tunnels, i.e. ‘mines’ on the leaves or stems (Dai et al. 2018, Eiseman 2020b, Liu et al. 2015, Sinclair and Hughes 2010). The mines can provide useful hints on insect species identities, insect life histories, insect behaviour and insect-plant interactions (Dai et al. 2018). Fewer miner groups (e.g. gracillariid moths, agromyzid flies and leaf-mining chrysomelids) can utilise over 100 plant families (Dai et al. 2017, De Prins and De Prins 2020, Santiago-Blay 2004, Spencer 1990), which are mainly angiosperm families, such as and (Dai et al. 2018).

Ferns (, including both and in the broad sense) are the second largest group of vascular plants, just after angiosperms (Dai et al. 2020, Schneider et al. 2004). With lower nutrition, higher defensive chemicals and no flowers, the interspecific associations between ferns and insects are often overlooked (Mehltreter et al. 2010, Weintraub et al. 1995). However, ferns used to be the primary food resource for insects before the thriving of angiosperms (Mehltreter et al. 2010). In fact, fossil records indicate that ferns and insects have co-evolved for at least 300 myr (Chandra and Srivastava 2003). Some ferns have nectaries and domatia, which could attract ants to be bodyguards (Mehltreter et al. 2010). Moreover, some insects mimic the soral crypsis of ferns to escape from their natural enemies (Barker et al. 2005, Patra et al. 2008). Some researchers hypothesise that fern-feeding insects should have fewer species, genera and families than those of seed plants (Weintraub et al. 1995), while others suggest that the richness of fern-feeding insects is largely underestimated (Auerbach and Hendrix 1980, Mehltreter et al. 2010). The possible underestimation might be deduced from the following facts: (1) many fewer investigations have been performed for wild ferns than for cultivated ferns or invasive ferns (Fountain-Jones et al. 2012); (2) many more fern herbivores have been discovered in the comprehensive screening of bio-control agents for pest ferns (Mehltreter et al. 2010); (3) no noticeable difference has been found between leaf herbivory loss of ferns and that of seed plants (Chandra and Srivastava 2003); and (4) the possible biases of plant apparency (i.e. body size, distribution range and individual numbers (Dai et al. 2017)) are not considered for phytophagous insects on ferns in comparison to those on seed plants (Auerbach and Hendrix 1980).

Fern-feeding insects could be classified as generalists and specialists. Most fern-feeding generalists tend to be classified as leaf-chewing or sap-sucking, while most specialists are classified as leaf-mining, gall-forming or spore-feeding (Mehltreter et al. 2010). By far, the miners on ferns are much less known than those on seed plants; although there are scattered records on publications and websites (De Prins and De Prins 2020, Edmunds et al. 2020, Ellis 2020, Eiseman 2020b, Pitkin et al. 2019, Santiago-Blay 2004, Spencer 1990), few comprehensive reviews on fern miners have been provided and a worldwide checklist has not been reported. In this study, we will compile a preliminary checklist of fern-mining insects and their host plants throughout the world, which could provide meaningful information to the study of plant-insect–environment interactions.

Material and methods

The names and hosts of fern miners were obtained from websites, books and articles. Most publications were retrieved from the Web of Science (https://www.webofknowledge.com) and Google Scholar (https://scholar.google.com), while the others were obtained from reference lists of the websites and retrieved publications. According to the Taxonomic Name Resolution Service (http://tnrs.iplantcollaborative.org/TNRSapp.html), the host fern's scientific names were verified and corrected. The number of species in a fern family was obtained from the Catalogue of Life (http://www.catalogueoflife.org/). Based on two recent mega-trees (Smith and Brown 2018, Zanne et al. 2014), 'GBOTB.extended.tre' is the latest and largest dated phylogenetic tree for vascular plants, with 74533 species, 10587 genera and all extant 479 families (Jin and Qian 2019). The R package 'V. PhyloMaker' (Jin and Qian 2019) can bind undetermined plant taxa to the backbone phylogeny of 'GBOTB.extended.tre' and generates the customised tree we needed (Dai et al. 2020). Here, we obtained the phylogenetic tree of our host fern families using the above method. Bivariate linear regression was fitted with Past 4.04 (Hammer et al. 2001).

Both leaf-miners and stem-borers have been found in the same insect family (e.g. , and ) or even in the same genus (e.g. , , and ) (Eiseman 2020b, Hering 1951, Shcherbakov 2006, Woodley and Janzen 1995). Occasionally, the same species could change their feeding habits from leaf-mining to stem-mining or stem-boring, when the younger larvae transform into the older larvae, when the leaf is too small to offer enough food or when leaves and stems do not differ significantly (Eiseman 2020b, Hering 1951). Such phenomena can be found in (= ) (), spp. (), spp. (), spp. (), (= ) (), (), () and many other species (Eiseman 2020b, Ellis 2020, Hering 1951, Kato 2002). There are transitions amongst leaf-mining, stem-mining, leaf-boring and stem boring (Hering 1951). Moreover, most ferns are herbaceous, with developed parenchyma in the stems (Crang et al. 2018). Therefore, we incorporated fern borers into fern miners for this article (Suppl. material 1). Some suspected insect species are not included in this study (e.g. Correia et al. 2020, Santiago-Blay 2004).

The miners' biogeographical regions followed Juan J. Morrone's system (Morrone 2002). For detailed information about fern miners associated with each host plant species, the original sources should be consulted.

Results

We recorded 128 species and 18 families of fern miners (Table 1; Suppl. material 2), including , , , , , , , , , , , , , , , , and . They were primarily distributed in the Palaearctic Region, Nearctic Region and Oriental Region of the Northern Hemisphere and the Neotropical Region between the Tropic of Cancer and the Tropic of Capricorn (Table 1). One explanation for this distribution pattern could be that the land area in the Northern Hemisphere is almost double that of the Southern Hemisphere. Another reason might be that the investigations on leaf-mining insects and their host plants are more thorough in the Northern than in the Southern Hemisphere (Sinclair and Hughes 2008, Sinclair and Hughes 2008, Sinclair and Hughes 2010).

Table 1.

A preliminary world checklist of fern miners and their biological information.

Miner family	Miner species	Host fern	Biogeographical regions	References
Diptera
Agromyzidae	Chromatomyia cheilanthus Garg*1	Cheilanthes virga-aure	Oriental Region	Spencer 1990
Agromyzidae	Chromatomyia dorsata Hendel2	Asplenium ceterach	Palaearctic Region	Ellis 2020, Spencer 1990
Agromyzidae	Chromatomyia dryoptericola Sasakawa3	Dryopteris lacera	Palaearctic Region	Sasakawa 2010, Spencer 1990
Agromyzidae	Chromatomyia dryoptericola Sasakawa	Asplenium pinnatifidum	Palaearctic Region
Agromyzidae	Chromatomyia dryoptericola Sasakawa	Lepisorus thunbergianus	Palaearctic Region
Agromyzidae	Chromatomyia masumiae Sasakawa	Lepisorus thunbergianus	Palaearctic Region	Sasakawa 2010
Agromyzidae	Chromatomyia scolopendri Robineau Desvoidy4	Asplenium ruta-muraria	Palaearctic Region	Civelek 2002, Dempewolf 2001, Ellis 2020, Sasakawa 2010, Spencer 1990
Agromyzidae	Chromatomyia scolopendri Robineau Desvoidy	Asplenium scolopendrium	Palaearctic Region
Agromyzidae	Chromatomyia scolopendri Robineau Desvoidy	Asplenium septentrionale	Palaearctic Region
Agromyzidae	Chromatomyia scolopendri Robineau Desvoidy	Polypodium vulgare	Palaearctic Region
Agromyzidae	Liriomyza equiseti de Meijere5	Equisetum arvense	Nearctic and Palaearctic Regions	Eiseman 2020b, Ellis 2020, George 2014, Lonsdale 2017, Spencer 1990
Agromyzidae	Liriomyza occipitalis Hendel6	Equisetum arvense	Palaearctic Region	Ellis 2020, George 2014, Spencer 1990
Agromyzidae	Liriomyza nordica Spencer*	Equisetum sp.	Nearctic Region	Eiseman 2020b
Agromyzidae	Liriomyza virgo Zetterstedt7	Equisetum fluviatile	Nearctic and Palaearctic Regions	Eiseman 2020b, Ellis 2020, George 2014, Lonsdale 2017, Spencer 1990
Agromyzidae	Liriomyza virgo Zetterstedt	Equisetum palustre	Nearctic and Palaearctic Regions
Agromyzidae	Liriomyza virgula Frey8	Equisetum arvense	Palearctic Regain	George 2014
Agromyzidae	Phytoliriomyza clara Melander	Pteridium aquilinum	Nearctic Region	Eiseman 2020b, Spencer 1990
Agromyzidae	Phytoliriomyza cyatheae Spencer	Cyathea dealbata	Neozelandic Region	Spencer 1976, Spencer 1990
Agromyzidae	Phytoliriomyza cyatheae Spencer	Cyathea smithii	Neozelandic Region
Agromyzidae	Phytoliriomyza diplazii Sasakawa	Diplazium	Oriental Region	Spencer 1990
Agromyzidae	Phytoliriomyza felti Malloch	Asplenium pinnatifidum	Nearctic Region	Eiseman 2020b, Spencer 1990
Agromyzidae	Phytoliriomyza felti Malloch	Asplenium platyneuron	Nearctic Region
Agromyzidae	Phytoliriomyza felti Malloch	Pellaea atropurpurea	Nearctic Region
Agromyzidae	Phytoliriomyza felti Malloch	Pellaea glabella	Nearctic Region
Agromyzidae	Phytoliriomyza felti Malloch	Asplenium rhizophyllum	Nearctic Region
Agromyzidae	Phytoliriomyza felti Malloch	Woodsia obtusa	Nearctic Region
Agromyzidae	Phytoliriomyza flavopleura Watt	Microsorum	Neozelandic Region	Spencer 1990
Agromyzidae	Phytoliriomyza flavopleura Watt	Notogrammitis billardierei	Neozelandic Region
Agromyzidae	Phytoliriomyza flavopleura Watt	Asplenium flaccidum	Neozelandic Region
Agromyzidae	Phytoliriomyza flavopleura Watt	Asplenium oblongifolium	Neozelandic Region
Agromyzidae	Phytoliriomyza hilarella Zetterstedt	Asplenium	Palaearctic Region	Ellis 2020, Lawton 1982, Lawton 1976, MacGarvin et al. 1986, Rigby and Lawton 1981, Spencer 1990
Agromyzidae	Phytoliriomyza hilarella Zetterstedt	Pteridium aquilinum	Palaearctic Region
Agromyzidae	Phytoliriomyza hilarella Zetterstedt	Polypodium	Palaearctic Region
Agromyzidae	Phytoliriomyza kuscheli Spencer	Histiopteris	Oriental Region	Spencer 1990
Agromyzidae	Phytoliriomyza pteridii Spencer	Pteridium aquilinum	Palaearctic Region	Gerson 1979, Mcgavin and Brown 1986, MacGarvin et al. 1986, Spencer 1990
Agromyzidae	Phytoliriomyza pulchella Spencer*	Pteridium aquilinum	Nearctic Region	Eiseman 2020b
Agromyzidae	Phytoliriomyza sp1	Marattia*	Oriental Region	Spencer 1990
Agromyzidae	Phytoliriomyza sp2	Cyathea	Neotropical andAndean Regions	Spencer 1990
Agromyzidae	Phytoliriomyza tearohensis Spencer	Cyathea dealbata	unknown	Spencer 1976, Spencer 1990
Agromyzidae	Tropicomyia angioptericola Shiao	Angiopteris lygodiifolia	Palaearctic Region	Shiao and Wu 2005
Agromyzidae	Tropicomyia polyphaga Spencer	Nephrolepis	Oriental Region	Spencer 1990, Shiao and Wu 2005
Agromyzidae	Tropicomyia sp1	Pleopeltis	Afrotopical Region	Spencer 1990
Agromyzidae	Tropicomyia sp1	Asplenium auriculatum	Afrotopical Region
Agromyzidae	Tropicomyia sp2	Angiopteris evecta*	Oriental Region	Spencer 1990
Anthomyiidae	Chirosia albifrons Tiens	Pteridium aquilinum	Palaearctic Region	Lawton 1976, MacGarvin et al. 1986
Anthomyiidae	Chirosia albitarsis Zetterstedt	Pteridium aquilinum	Palaearctic and Oriental Regions	Ellis 2020, Gerson 1979, Lawton 1976, Mcgavin and Brown 1986, Suwa 1984, Suwa 1999
Anthomyiidae	Chirosia asperistilata Suwa	Dryopteris monticola	Palaearctic Region	Suwa 1999, Suwa 2005
Anthomyiidae	Chirosia asperistilata Suwa	Dryopteris crassirhizoma	Palaearctic Region
Anthomyiidae	Chirosia cinerosa Zetterstedt9	Pteridium aquilinum	Palaearctic Region	Ellis 2020, Kwon and Suh 1982, Suwa 1999
Anthomyiidae	Chirosia cinerosa Zetterstedt	Matteuccia struthiopteris	Palaearctic Region
Anthomyiidae	Chirosia cinerosa Zetterstedt	Athyrium filix-femina	Palaearctic Region
Anthomyiidae	Chirosia crassiseta Stein	Pteridium aquilinum	Palaearctic Region	Brown and McGavin 2007, Ellis 2020, Gerson 1979, Lawton 1976, Mcgavin and Brown 1986
Anthomyiidae	Chirosia filicis Huckett	Osmunda claytoniana	Nearctic Region	Eiseman 2018, Eiseman 2020b
Anthomyiidae	Chirosia filicis Huckett	Osmundastrum cinnamomeum	Nearctic Region
Anthomyiidae	Chirosia flavipennis Fallen	Pteridium aquilinum	Nearctic and Palaearctic Regions	Eiseman 2020b, Eiseman 2018, Lawton 1976, Suwa 2013
Anthomyiidae	Chirosia gleniensis Huckett	Onoclea sensibilis	Nearctic Region	Eiseman 2020b, Eiseman 2018, Eiseman 2020a
Anthomyiidae	Chirosia gleniensis Huckett	Woodsia areolata	Nearctic Region
Anthomyiidae	Chirosia gleniensis Huckett	Woodsia virginica*	Nearctic Region
Anthomyiidae	Chirosia griseifrons Séguy	Dryopteris*	Palaearctic Region	Ellis 2020, Suwa 1999
Anthomyiidae	Chirosia griseifrons Séguy	Athyrium filix-femina	Palaearctic Region
Anthomyiidae	Chirosia grossicauda Strobl10	Asplenium	Palaearctic Region	Ellis 2020, Gerson 1979, Lawton 1976, MacGarvin et al. 1986, Mcgavin and Brown 1986, Suwa 1999
Anthomyiidae	Chirosia grossicauda Strobl	Pteridium aquilinum	Palaearctic Region
Anthomyiidae	Chirosia grossicauda Strobl	Dryopteris*	Palaearctic Region
Anthomyiidae	Chirosia histricina Rondani11	Osmunda regalis	Nearctic andPalaearctic Regions	Brown and McGavin 2007, Ellis 2020, MacGarvin et al. 1986, Mcgavin and Brown 1986, Suwa 1999
Anthomyiidae	Chirosia histricina Rondani	Asplenium	Nearctic andPalaearctic Regions
Anthomyiidae	Chirosia histricina Rondani	Blechnum spicant	Nearctic andPalaearctic Regions
Anthomyiidae	Chirosia histricina Rondani	Pteridium aquilinum	Nearctic andPalaearctic Regions
Anthomyiidae	Chirosia histricina Rondani	Dryopteris filix-mas	Nearctic andPalaearctic Regions
Anthomyiidae	Chirosia histricina Rondani	Matteuccia struthiopteris	Nearctic andPalaearctic Regions
Anthomyiidae	Chirosia histricina Rondani	Polypodium	Nearctic andPalaearctic Regions
Anthomyiidae	Chirosia histricina Rondani	Athyrium filix-femina	Nearctic andPalaearctic Regions
Anthomyiidae	Chirosia histricina Rondani	Cystopteris fragilis	Nearctic andPalaearctic Regions
Anthomyiidae	Chirosia montana Pokorny	Cystopteris fragilis	Nearctic and Palaearctic Regions	Eiseman 2020b, Eiseman 2018
Anthomyiidae	Chirosia nigripes Bezzi	Pteridium aquilinum	Palaearctic Region	Ellis 2020, Suwa 1999
Anthomyiidae	Chirosia pusillans Huckett	Athyrium filix-femina	Nearctic Region	Eiseman 2018, Eiseman 2020a, Eiseman 2020b
Anthomyiidae	Chirosia pusillans Huckett	Matteuccia struthiopteris	Nearctic Region
Anthomyiidae	Chirosia spinosissima Malloch	Pteridium aquilinum	Nearctic and Palaearctic Regions	Eiseman 2020b, Eiseman 2020a
Anthomyiidae	Pegomya cedrica Huckett	Equisetum hyemale	Nearctic Region	Michelsen and Palmer 2020
Anthomyiidae	Pegomya disticha Griffiths	Equisetum hyemale	Nearctic Region	Michelsen and Palmer 2020
Anthomyiidae	Pegomya glabra Stein	Equisetum	Nearctic Region	Michelsen and Palmer 2020
Drosophilidae	Drosophila apicipuncta Hardy	Sadleria	Nearctic Region	Magnacca et al. 2008, Magnacca and O'Grady 2014, Maunsell et al. 2016
Drosophilidae	Drosophila diminuens Hardy*	Sadleria	Nearctic Region	Magnacca and O'Grady 2014
Drosophilidae	Drosophila sadleria Bryan	Sadleria	Nearctic Region	Magnacca et al. 2008
Drosophilidae	Scaptodrosophila notha Bock	Pteridium aquilinum	Australotropical and Australotemperate Regions	Maunsell et al. 2016
Drosophilidae	Scaptodrosophila sp.	Parablechnum wattsii	Australotropical and Australotemperate Regions	Maunsell et al. 2016
Chironomidae	Bryophaenocladius furcatus Kieffer	Adiantum	Nearctic and Palaearctic Regions	Eiseman 2020b
Pallopteridae	Temnosira czurhini Ozerov	Huperzia serrata	Palaearctic Region	Kato 2002
Lepidoptera
Crambidae	Albusambia elaphoglossumae Solis & Davis	Elaphoglossum conspersum	Nearctic Region	Solis et al. 2005a
Crambidae	Albusambia elaphoglossumae Solis & Davis	Elaphoglossum biolleyi	Nearctic Region
Crambidae	Eudonia zophoclaena Meyrick	Pyrrosia eleagnifolia	Neozelandic Region	Patrick 2015
Crambidae	Scoparia illota Philpott	Pyrrosia eleagnifolia	Neozelandic Region	Patrick 2015
Crambidae	Scoparia molifera Meyrick	Pyrrosia eleagnifolia	Neozelandic Region	Patrick 2015
Crambidae	Siamusotima aranea Solis & Yen	Lygodium flexuosum	Oriental Region	Solis et al. 2005b
Crambidae	Siamusotima disrupta Solis	Lygodium	Palaearctic Region	Solis et al. 2017
Crambidae	Undulambia polystichalis Capps	Rumohra adiantiformis	Nearctic Region	Gerson 1979
Noctuidae	Hydraecia micacea Esper	Equisetum	Palearctic Region	Ellis 2020
Noctuidae	Papaipema inquaesita Grote & Robinson	Onoclea sensibilis	Nearctic Region	Bird 2012
Noctuidae	Papaipema pterisii Bird	Pteridium aquilinum	Nearctic Region	Bird 2012, Hinz and Zahniser 2015Schweitzer 2012
Noctuidae	Papaipema pterisii Bird	Matteuccia struthiopteris*	Nearctic Region
Noctuidae	Papaipema speciosissima Grote & Robinson	Osmunda regalis	Nearctic Region	Hinz and Zahniser 2015, Lafontaine and Schmidt 2010, Oppenheim et al. 2018
Noctuidae	Papaipema speciosissima Grote & Robinson	Osmundastrum cinnamomeum	Nearctic Region
Noctuidae	Papaipema stenocelis Dyar	Woodwardia virginica	Nearctic Region	Chaloux, Andrea 2012
Noctuidae	Pseudobryomima fallax Hampson	Pellaea andromedifolia	Nearctic Region	Eiseman 2020b
Noctuidae	Pseudobryomima muscosa Hampson	Polypodium californicum	Nearctic Region	Eiseman 2020b
Tineidae	Psychoides filicivora Meyrick12	Asplenium adiantum-nigrum	Palaearctic Region	Gaedike 2019, Kim and Bae 2007
Tineidae	Psychoides filicivora Meyrick	Asplenium ceterach	Palaearctic Region
Tineidae	Psychoides filicivora Meyrick	Asplenium scolopendrium	Palaearctic Region
Tineidae	Psychoides filicivora Meyrick	Asplenium trichomanes	Palaearctic Region
Tineidae	Psychoides filicivora Meyrick	Dryopteris filix-mas	Palaearctic Region
Tineidae	Psychoides filicivora Meyrick	Dryopteris aculeata	Palaearctic Region
Tineidae	Psychoides filicivora Meyrick	Polystichum setiferum	Palaearctic Region
Tineidae	Psychoides gosari Kim & Bae	Athyrium yokoscense	Oriental and Palaearctic Regions	Kim and Bae 2007
Tineidae	Psychoides gosari Kim & Bae	Dryopteris setosa	Oriental and Palaearctic Region
Tineidae	Psychoides gosari Kim & Bae	Dryopteris chinensis	Oriental and Palaearctic Regions
Tineidae	Psychoides gosari Kim & Bae	Dryopteris crassirhizoma	Oriental and Palaearctic Regions
Tineidae	Psychoides gosari Kim & Bae	Dryopteris saxifraga	Oriental and Palaearctic Regions
Tineidae	Psychoides phaedrospora Meyrick13	Aspleniaceae	Palaearctic and Oriental Regions	Gaedike 2019, Kim and Bae 2007
Tineidae	Psychoides verhuella Bruand14	Asplenium ceterach	Palaearctic Region	Ellis 2020, Gaedike 2019, Heckford 2004, Kim and Bae 2007, Muus 2015
Tineidae	Psychoides verhuella Bruand	Asplenium ruta-muraria	Palaearctic Region
Tineidae	Psychoides verhuella Bruand	Asplenium scolopendrium	Palaearctic Region
Tineidae	Psychoides verhuella Bruand	Asplenium trichomanes	Palaearctic Region
Tineidae	Psychoides verhuella Bruand	Pteridium aquilinum	Palaearctic Region
Tortricidae	Apoctena taipana Felder & Rogenhofer	Pyrrosia eleagnifolia	Neozelandic Region	Patrick 2015
Tortricidae	Celypha tiedemanniana Zeller15	Equisetum	Palaearctic Region	Ellis 2020
Tortricidae	Philocryptica polypodii Watt	Pyrrosia eleagnifolia	Neozelandic Region	Patrick 2015
Cosmopterigidae	Hyposmocoma (Euperissus) ekaha Swezey	Asplenium nidus	Oriental Region	Kawahara et al. 2011
Cosmopterigidae	Hyposmocoma (Euperissus) trivitella Swezey	Elaphoglossum aemulum	Oriental Region	Kawahara et al. 2011
Cosmopterigidae	Hyposmocoma (Euperissus) trivitella Swezey	Elaphoglossum gorgoneum	Oriental Region
Cosmopterigidae	Hyposmocoma (Euperissus) trivitella Swezey	Elaphoglossum crassifolium	Oriental Region
Cosmopterigidae	Hyposmocoma (Euperissus) trivitella Swezey	Elaphoglossum reticulatum	Oriental Region
Gelechiidae	Monochroa harrisonella Busck	Pteridium aquilinum	Nearctic Region	Eiseman 2020b
Gelechiidae	Paltodora cytisella Curti	Pteridium aquilinum	Palaearctic Region	Lawton 1976, Rigby and Lawton 1981
Hepialidae	Endoclita excrescens Butler*	Equisetum arvense	Palaearctic Region	Correia et al. 2020, Grehan 1989
Hepialidae	Triodia sylvina Linnaeus*	Equisetum arvense	Palaearctic Region	Correia et al. 2020, Grehan 1989
Psychidae	Apterona helicoidella Vallot	Polypodium	unknown	Alders and Gielis 1999
Hymenoptera
Blasticotomidae	Blasticotoma atra Zhelochovtsev	unknown	unknown	Taeger et al. 2010, Wikipedia 2019
Blasticotomidae	Blasticotoma filiceti Klug	Pteridium aquilinum	Palaearctic Region	Ellis 2020, Liston 2007, Novgorodova and Biryukova 2011, Shcherbakov 2006, Shcherbakov 2008, Taeger et al. 2010, Wikipedia 2019
Blasticotomidae	Blasticotoma filiceti Klug	Dryopteris	Palaearctic Region
Blasticotomidae	Blasticotoma filiceti Klug	Polystichum	Palaearctic Region
Blasticotomidae	Blasticotoma filiceti Klug	Matteuccia struthiopteris	Palaearctic Region
Blasticotomidae	Blasticotoma filiceti Klug	Athyrium alpestre	Palaearctic Region
Blasticotomidae	Blasticotoma filiceti Klug	Athyrium filix-femina	Palaearctic Region
Blasticotomidae	Blasticotoma filiceti var. pacificus Malaise	unknown	unknown	Taeger et al. 2010, Wikipedia 2019
Blasticotomidae	Blasticotoma nipponica Takeuchi	unknown	unknown	Wikipedia 2019, Taeger et al. 2010
Blasticotomidae	Blasticotoma smithi Shinohara	unknown	unknown	Taeger et al. 2010, Wikipedia 2019
Blasticotomidae	Blasticotoma warabii Togashi	unknown	unknown	Taeger et al. 2010, Wikipedia 2019
Blasticotomidae	Bohea abrupta Maa	unknown	unknown	Taeger et al. 2010, Wikipedia 2019
Blasticotomidae	Paremphytus ostentus Brues	unknown	unknown	Taeger et al. 2010, Wikipedia 2019
Blasticotomidae	Runaria flavipes Takeuchi	unknown	unknown	Taeger et al. 2010, Wikipedia 2019
Blasticotomidae	Runaria hunannica Wei in Wei & Nie	unknown	unknown	Taeger et al. 2010, Wikipedia 2019
Blasticotomidae	Runaria punctata Wei in Wei & Nie	unknown	unknown	Taeger et al. 2010, Wikipedia 2019
Blasticotomidae	Runaria shaanxinica Wei in Wei & Nie	unknown	unknown	Taeger et al. 2010, Wikipedia 2019
Blasticotomidae	Runaria taiwana Shinohara	unknown	unknown	Taeger et al. 2010, Wikipedia 2019
Tenthredinidae	Aneugmenus coronatus Klug	Pteridium aquilinum	Palaearctic Region	Beneš 2014, Ellis 2020, Schwarz 2005
Tenthredinidae	Aneugmenus coronatus Klug	Dryopteris filix-mas	Palaearctic Region
Tenthredinidae	Aneugmenus coronatus Klug	Polystichum setiferum	Palaearctic Region
Tenthredinidae	Aneugmenus coronatus Klug	Athyrium filix-femina	Palaearctic Region
Tenthredinidae	Heptamelus dahlbomi Thomson	Athyrium filix-femina	Nearctic and Palaearctic Regions	Vikberg and Liston 2009
Tenthredinidae	Heptamelus ochroleucus Stephens16	Blechnum spicant	Nearctic andPalaearctic Regions	Ellis 2020, Shcherbakov 2008, Vikberg 2017, Vikberg and Liston 2009
Tenthredinidae	Heptamelus ochroleucus Stephens	Matteuccia struthiopteris	Nearctic andPalaearctic Regions
Tenthredinidae	Heptamelus ochroleucus Stephens	Dryopteris dilatata	Nearctic andPalaearctic Regions
Tenthredinidae	Heptamelus ochroleucus Stephens	Polypodium vulgare	Nearctic andPalaearctic Regions
Tenthredinidae	Heptamelus ochroleucus Stephens	Athyrium filix-femina	Nearctic andPalaearctic Regions
Coleoptera
Buprestidae	Endelus bakerianus Obenberger	Lygodium microphyllum	Oriental Region	Kalashian 2013, Goolsby et al. 2003, Mehltreter et al. 2010
Buprestidae	Neotrachys bellamyi Hespenheide	Gleichenia glauca	Neotropical Region	Hespenheide 2006
Buprestidae	Neotrachys bicolor Hespenheide	Cnemidaria petiolata	Neotropical Region	Hespenheide 1982
Buprestidae	Neotrachys bordoni Cobos	Cyatheaceae	Neotropical Region	Hespenheide 1982
Buprestidae	Neotrachys caerulea Hespenheide	Cyatheaceae	Neotropical Region	Hespenheide 1982
Buprestidae	Neotrachys concinna Fisher	Cyatheaceae	Neotropical Region	Hespenheide 1982, Hespenheide 2006
Buprestidae	Neotrachys cyanipennis Fisher	Cyatheaceae	Neotropical Region	Hespenheide 2006
Buprestidae	Neotrachys estebana Kerremans*	Dicranopteris	Neotropical Region	Hespenheide 1982
Buprestidae	Neotrachys fennahi Thery	Cyatheaceae	Neotropical Region	Hespenheide 1980
Buprestidae	Neotrachys gleicheniae Hespenheide	Gleichenia	Neotropical Region	Hespenheide 1982
Buprestidae	Neotrachys hoffmani Fisher	Cyatheaceae	Neotropical Region	Hespenheide 1980, Hespenheide 1982
Buprestidae	Neotrachys mariae Hespenheide	Gleichenia	Neotropical Region	Hespenheide 2006
Buprestidae	Neotrachys resplendens Hespenheide	Cyatheaceae	Neotropical Region	Hespenheide 1982
Buprestidae	Neotrachys segregata Waterhouse	Gleicheniaceae*	Neotropical Region	Hespenheide 1982
Buprestidae	Neotrachys solisi Hespenheide	Gleichenia	Neotropical Region	Hespenheide 2006
Chrysomelidae	Febra insularis Bryant	Acrostichum aureum	Oriental Region	Samuelson 1973, Santiago-Blay 2004
Chrysomelidae	Febra ovata Bryant	Angiopteris evecta	Oriental Region	Samuelson 1973, Nadein 2013, Jolivet 1991
Chrysomelidae	Febra venusta Clark	Nephrolepis	Oriental Region	Samuelson 1973, Santiago-Blay 2004
Chrysomelidae	Halticorcus bhaumiki Basu et Sengupta17	Pteris vittata	Palaearctic and Oriental Regions	Isowa and Kojima 2011, Konstantinov and Prathapan 2008, Patra and Bera 2007
Chrysomelidae	Halticorcus bhaumiki Basu et Sengupta	Ampelopteris prolifera	Palaearctic and Oriental Regions
Chrysomelidae	Halticorcus bhaumiki Basu et Sengupta	Cyclosorus	Palaearctic and Oriental Regions
Chrysomelidae	Halticorcus bhaumiki Basu et Sengupta	Christella dentata	Palaearctic and Oriental Regions
Chrysomelidae	Halticorcus bhaumiki Basu et Sengupta	Nephrolepis cordifolia	Palaearctic and Oriental Regions
Chrysomelidae	Halticorcus bhaumiki Basu et Sengupta	Nephrolepis exaltata	Palaearctic and Oriental Regions
Chrysomelidae	Halticorcus bhaumiki Basu et Sengupta	Adiantum lunulatum	Palaearctic and Oriental Regions
Chrysomelidae	Halticorcus bhaumiki Basu et Sengupta	Drynaria propinqua	Palaearctic and Oriental Regions
Chrysomelidae	Halticorcus bhaumiki Basu et Sengupta	Pyrrosia adnascens	Palaearctic and Oriental Regions
Chrysomelidae	Halticorcus bhaumiki Basu et Sengupta	Microsorum scolopendria	Palaearctic and Oriental Regions
Chrysomelidae	Halticorcus hiranoi Takizawa18	Lemmaphyllum microphyllum	Palaearctic Region	Kato 1991, Santiago-Blay 2004
Chrysomelidae	Halticorcus hiranoi Takizawa	Loxogramme salicifolia*	Palaearctic Region
Chrysomelidae	Halticorcus kasuga Nakane	Lepisorus thunbergianus	Palaearctic Region	Isowa and Kojima 2011
Chrysomelidae	Halticorcus kasuga Nakane	Lepisorus onoei	Palaearctic Region
Chrysomelidae	Halticorcus kasuga Nakane	Lemmaphyllum microphyllum	Palaearctic Region
Chrysomelidae	Halticorcus kasuga Nakane	Pyrrosia linearifolia	Palaearctic Region
Chrysomelidae	Halticorcus platyceriiLea	Platycerium alcicorne	Australotropical, Australotemperate and Palaearctic Regions	Hawkeswood 2003, Isowa and Kojima 2011, Sinclair and Hughes 2010
Chrysomelidae	Halticorcus platyceriiLea	Asplenium nidus	Australotropical, Australotemperate and Palaearctic Regions
Chrysomelidae	Halticorcus sauteri Chen19	Colysis elliptica	Palaearctic Region	Kato 1991, Santiago-Blay 2004
Chrysomelidae	Halticorcus sauteri Chen	Leptochilus ellipticus	Palaearctic Region
Chrysomelidae	Hippuriphila babai Chujo*	Equisetum	Palaearctic Region	Correia et al. 2020, Poinar 2014
Chrysomelidae	Hippuriphila canadensis Brown*	Equisetum arvense	Nearctic Region	Correia et al. 2020, Poinar 2014
Chrysomelidae	Hippuriphila catherinae Barr*	Equisetum	Neotropical Region	Correia et al. 2020, Poinar 2014
Chrysomelidae	Hippuriphila equiseti Beller et Hatch*	Equisetum arvense	Nearctic Region	Correia et al. 2020, Poinar 2014
Chrysomelidae	Hippuriphila modeeri Linnaeus	Equisetum arvense	Palaearctic Region	Biological Records Centre 2020, Ellis 2020, Santiago-Blay 2004
Chrysomelidae	Hippuriphila modeeri Linnaeus	Equisetum fluviatile	Palaearctic Region
Chrysomelidae	Hippuriphila modeeri Linnaeus	Equisetum palustre	Palaearctic Region
Curculionidae	Bagous claudicans Boheman	Equisetum fluviatile	except for Central and South America, all the world	Ellis 2020, Gosik et al. 2019
Curculionidae	Bagous lutulentus Gyllenhal20	Equisetum fluviatile	except for Central and South America, all the world	Ellis 2020, Gosik 2009, Gosik et al. 2019, Gosik and Wanat 2014
Curculionidae	Grypus brunnirostris Fabricius21	Equisetum arvense	Nearctic Region	Ellis 2020, George 2014
Curculionidae	Grypus brunnirostris Fabricius	Equisetum fluviatile	Nearctic Region
Curculionidae	Grypus brunnirostris Fabricius	Equisetum ramosissimum	Nearctic Region
Curculionidae	Grypus equiseti Fabricius22	Equisetum arvense	Nearctic and Palaearctic Regions	Ellis 2020, George 2014, Gosik et al. 2019
Curculionidae	Grypus equiseti Fabricius	Equisetum palustre	Nearctic and Palaearctic Regions
Curculionidae	Grypus equiseti Fabricius	Equisetum pratense	Nearctic and Palaearctic Regions
Curculionidae	Grypus equiseti Fabricius	Equisetum sylvaticum	Nearctic and Palaearctic Regions
Curculionidae	Stenopelmus rufinasus Gyllenhal	Azolla	Nearctic, Afrotopical and Palaearctic Regions	Center et al. 2002, Hill and Cilliers 1999, Richerson and Grigarick 1967

* possible host fern or miner

Synonyms:

1 Garg = Garg;

2 Hendel = Hendel;

3 Sasakawa = Sasakawa

4 Robineau-Desvoidy = = Goureau = Strobl = Strobl;

5 de Meijere = Spencer;

6 Hendel = Hering;

7 Zetterstedt = Spencer = Zetterstedt;

8 Frey = Hering;

9 Zetterstedt = Zetterstedt;

10 Strobl = nec Zetterstedt;

11 Rondani = Ringdahl = Brischke = ;

12 Meyrick = Meyrick;

13 Meyrick = Meyrick;

14 Bruand = Herrich-Schaffer = Stainton;

15 Zeller = Zeller Kuznetsov = Zeller;

16 Stephens = Stephens;

17 Basu et Sengupta = Basu and Sengupta;

18 Takizawa = Takizawa;

19 Chen = Chen;

20 Gyllenhal = Thomson;

21 Fabricius = Curculio Inspectionatus Herbst;

22 Fabricius = Fabricius;

Fern miners belong to four orders: (51 species; 39.8%), (33 species; 25.8%), (28 species; 21.9%) and (16 species; 12.5%) (Fig. 1; Suppl. material 2). In general, dipteran leaf miners are dominant in herbaceous plants while lepidopteran leaf miners are dominant in woody plants (De Prins and De Prins 2020, Edmunds et al. 2020, Eiseman 2020b, Ellis 2020, Pitkin et al. 2019, Spencer 1990). The life form of most extant ferns is herbaceous, which could explain why nearly half of fern-mining species are dipteran flies.

Figure 1.

Percentage distribution of the fern-mining species into the four orders and the 18 families.

Amongst the 18 fern-mining insect families, , , , and had the highest numbers of species (20.3%, 14.1%, 11.7%, 10.2% and 10.2%, respectively), while the other 13 families accounted for 33.5% only (Fig. 1; Suppl. material 2).

The fern families with highest numbers of host species were (19), (18) and (15) (Fig. 2; Suppl. material 3). The fern families with the highest numbers of miner species were (21), (21), (20) and (14) (Fig. 2; Suppl. material 3). With 82 species and 12 families of host ferns and 67 species of fern miners, was the dominant host order of fern-mining insects (Suppl. material 3).

Figure 2.

The dated phylogenetic tree of host fern families generated with the R package 'V. PhyloMaker' (Jin and Qian 2019). The first number after the fern family is the number of host fern species and the second is the number of fern miner species. The length of each branch is also shown and the scale bar unit is 100 myr.

The number of host species was significantly and positively correlated with the total number of fern species at the family level (R2 = 0.614, t = 5.352, P < 0.001; Fig. 3a), but the number of miner species was not significantly correlated with the total number of fern species at the family level (R2 = 0.110, t = 1.495, P = 0.152; Fig. 3b).

Figure 3a.

Figure 3b.

Discussion

In this paper, we provide a preliminary checklist about fern miners and their host plants worldwide. Table 1 summarises this checklist in terms of published information to date. However, there is also more information available on some fern-mining groups and this is summarised here:

(1) : In , there is an unknown species with as host in the Nearctic Region (Eiseman 2020b), while could be a possible Nearctic borer (Eiseman 2018). In , the Fuscoamoeba subgroup has many species that have been reared from rotting fern rachises (Magnacca et al. 2008). For species in , Kahanpää (2014) separates and as different genera (Kahanpää 2014) and Spencer (1990) considers that should belong to the genus (Spencer 1990). Molecular phylogeny suggests that the genus of should include all species of , , and (Winkler et al. 2009). However, only one fern-feeding species is included in the above molecular analysis. Moreover, no s. s. species has previously been found as fern-mining. In this article, we rather kept the genus name of and listed the species as the synonym of the corresponding species in Table 1.

(2) : In , early instar larvae of the subfamily are leaf miners, while their later instars feed on sporangia from a loose portable case (Gaedike 2019). An unknown species of has two hosts ( and ) in the Oriental Region (Goolsby et al. 2003). There is an unknown moth in the Nearctic Region, which mines the leaves of (Eiseman 2020b), but the species name could not be confirmed. In , larvae make gall-like deformities on the fronds of the bracken () (Eiseman 2020b). Eiseman (personal observations) believes that the deformities are caused by internal feeding; he has also reared an undetermined species from larvae that similarly bored in the terminal part of the rachis and caused a gall-like deformity.

(3) : In , the genus has 36 species in the Palaearctic and Oriental Regions and their larvae are internal feeders and all probably use ferns as larva hosts (Vikberg and Liston 2009), but we cannot know with certainty which species of is involved, except for on (Vikberg 2017). With only 13 species and 3 tribes in Eurasia's temperate region, is a small family in the and their larvae are stem borers on ferns (Taeger et al. 2010, Wikipedia 2019, Santiago-Blay 2004).

(4) : In , both and have fern-mining habits (Xiao 2018, Bellamy 1997). Most feed on the ferns of and (Hespenheide 1980, Hespenheide 1982, Hespenheide 2006). However, some larvae may mine other non-fern plants. For example, feeds on () (Meurgey 2017). The genus is morphologically similar and sometimes confused with , but feeds on and (Hespenheide 1991). Fern-feeding or not could be a clue to distinguish and its related genera. Although there are many publications on , only very few mention its host plants (Kalashian 2013).

Dominant plant groups generally are rich in leaf miners and rich in host plants, which could be explained by the ‘plant apparency hypothesis’ (Feeny 1976). Such phenomena have been found in several other leaf-mining insects (Dai et al. 2017, Dai et al. 2018). Apart from species richness in a fern taxonomic group, the distribution range should also be considered as an important component of 'plant apparency' (Dai et al. 2017). has 39 species and eight host species, and has 245 species and two host species, but both families host 21 miner species, which is the highest amongst all fern families (Fig. 2; Suppl. material 3). It is and that strongly affected the significance of the correlation in Fig. 3b. In particular, the bracken fern (), one species in , had 20 miner species (Suppl. material 3), which is not less than many dominant flowering plants. The bracken fern might be the only globally distributed fern and one of the most widespread vascular plants, which occurs in temperate and subtropical regions in both hemispheres (Flora of North America Editorial Committee 1993). It is used as vegetable, food or feed in many places. It is also a common invasive plant in disturbed areas (Flora of North America Editorial Committee 1993). The above features of the bracken fern make it highly attractive to both miners and researchers, thus the high number of mining species might be the combined effects of plant apparency and sampling effects. has 2257 species (Suppl. material 3) and also a cosmopolitan distribution, with many cultivated ornamental species (Olsen and Olsen 2007). has 855 species (Suppl. material 3) and also a worldwide distribution (POWO 2019). has 1667 species (Suppl. material 3) and is distributed nearly worldwide, but mainly in tropical areas, with some cultivated species (Simpson 2010). Both high species richness and wide geographical distribution could explain why the three families have large numbers of both host fern species and miner species. Besides , (), () and () also have a high richness of miners (10, 8 and 6 species, respectively) (Suppl. material 3). The common horsetail () is native throughout the Arctic and temperate regions in the Northern Hemisphere (Schaffner 1930). becomes an invasive plant in New Zealand and a systematic evaluation of its potential biocontrol agents including miners and borers has been performed (Paynter and Barton 2008). The common lady-fern () is one of the most abundant fern species in the temperate regions in the Northern Hemisphere (Adam 1995). The ostrich fern () is widely distributed in the temperate regions of the Northern Hemisphere (Kimura et al. 2004). However, since the checklist of fern-mining insects and the corresponding host fern species is preliminary, these patterns need further verification.

As the sampling of fern miners and their hosts are insufficient in many places and some sampled records might be inaccessible, this study was only a preliminary list. We hope that this basic list can serve as an inital reference for future inventories and research on fern-mining insects.

The feeding mode and feeding plant organ of each fern miner

Feeding habits

File: oo_522267.xlsx

The number of fern-miners in each insect family and each insect order

Number of species

File: oo_522268.xlsx

The number of miners on each fern species, each fern family and each fern order

Number of species

File: oo_522269.xlsx