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Research Article
A preliminary world checklist of fern-mining insects
expand article infoJie Yang, Xuexiong Wang, Kevin Jan Duffy§, Xiaohua Dai‡,|
‡ Leafminer Group, School of Life Sciences, Gannan Normal University, Ganzhou, China
§ Institute of Systems Science, Durban University of Technology, Durban, South Africa
| National Navel-Orange Engineering Research Center, Ganzhou, China
Open Access

Abstract

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.

Keywords

fern, leaf miner, host plant, plant-insect interactions, plant apparency hypothesis

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 Fagaceae and Myrtaceae (Dai et al. 2018).

Ferns (Pteridophyta, including both Lycopodiophyta and Polypodiophyta 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. Buprestidae, Cossidae and Blasticotomidae) or even in the same genus (e.g. Amauromyza, Melanagromyza, Phytomyza and Zygoneura) (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 Heliozela hammoniella (= Heliozela betulae) (Heliozelidae), Marmara spp. (Gracillariidae), Ophiomyia spp. (Agromyzidae), Phyllocnistis spp. (Gracillariidae), Scaptomyza graminum (= Scaptomyzella incana) (Drosophilidae), Zygoneura calthella (Sciaridae), Temnosira czurhini (Pallopteridae) 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 Agromyzidae, Anthomyiidae, Drosophilidae, Chironomidae, Pallopteridae, Buprestidae, Chrysomelidae, Curculionidae, Crambidae, Noctuidae, Tineidae, Tortricidae, Cosmopterigidae, Gelechiidae, Hepialidae, Psychidae, Blasticotomidae and Tenthredinidae. 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 and

Andean 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 and

Palaearctic Regions

Brown and McGavin 2007, Ellis 2020, MacGarvin et al. 1986, Mcgavin and Brown 1986, Suwa 1999

Anthomyiidae

Chirosia histricina Rondani

Asplenium

Nearctic and

Palaearctic Regions

Anthomyiidae

Chirosia histricina Rondani

Blechnum spicant

Nearctic and

Palaearctic Regions

Anthomyiidae

Chirosia histricina Rondani

Pteridium aquilinum

Nearctic and

Palaearctic Regions

Anthomyiidae

Chirosia histricina Rondani

Dryopteris filix-mas

Nearctic and

Palaearctic Regions

Anthomyiidae

Chirosia histricina Rondani

Matteuccia struthiopteris

Nearctic and

Palaearctic Regions

Anthomyiidae

Chirosia histricina Rondani

Polypodium

Nearctic and

Palaearctic Regions

Anthomyiidae

Chirosia histricina Rondani

Athyrium filix-femina

Nearctic and

Palaearctic Regions

Anthomyiidae

Chirosia histricina Rondani

Cystopteris fragilis

Nearctic and

Palaearctic 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 2015 Schweitzer 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 and

Palaearctic Regions

Ellis 2020, Shcherbakov 2008, Vikberg 2017, Vikberg and Liston 2009

Tenthredinidae

Heptamelus ochroleucus Stephens

Matteuccia struthiopteris

Nearctic and

Palaearctic Regions

Tenthredinidae

Heptamelus ochroleucus Stephens

Dryopteris dilatata

Nearctic and

Palaearctic Regions

Tenthredinidae

Heptamelus ochroleucus Stephens

Polypodium vulgare

Nearctic and

Palaearctic Regions

Tenthredinidae

Heptamelus ochroleucus Stephens

Athyrium filix-femina

Nearctic and

Palaearctic 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 platycerii

Lea

Platycerium alcicorne

Australotropical, Australotemperate and Palaearctic Regions

Hawkeswood 2003, Isowa and Kojima 2011, Sinclair and Hughes 2010

Chrysomelidae

Halticorcus platycerii

Lea

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 Chromatomyia cheilanthus Garg = Phytomyza cheilanthus Garg;

2 Chromatomyia dorsata Hendel = Phytomyza dorsata Hendel;

3 Chromatomyia dryoptericola Sasakawa = Phytomyza dryoptericola Sasakawa

4 Chromatomyia scolopendri Robineau-Desvoidy = Phytomyza scolopendri Goureau = Phytomyza elegans Goureau = Phytomyza nevadensis Strobl = Chromatoinyia nevadensis Strobl;

5 Liriomyza equiseti de Meijere = Liriomyza kenti Spencer;

6 Liriomyza occipitalis Hendel = Liriomyza bruscae Hering;

7 Liriomyza virgo Zetterstedt = Liriomyza arcticola Spencer = Phytomyza pallicornis Zetterstedt;

8 Liriomyza virgula Frey = Liriomyza larissa Hering;

9 Chirosia cinerosa Zetterstedt = Pycnoglossa cinerosa Zetterstedt;

10 Chirosia grossicauda Strobl = Chirosia parvicornis nec Zetterstedt;

11 Chirosia histricina Rondani = Chirosia setifemur Ringdahl = Pycnoglossa hystrix Brischke = Pycnoglossa hystricina;

12 Psychoides filicivora Meyrick = Teichobia filicivora Meyrick;

13 Psychoides phaedrospora Meyrick = Mnesipatris phadrospora Meyrick;

14 Psychoides verhuella Bruand = Teichobia verhuellella Herrich-Schaffer = Lambrosetia verhuellella Stainton;

15 Celypha tiedemanniana Zeller = Olethreutes tiedemanniana Zeller Kuznetsov = Syricoris tiedemanniana Zeller;

16 Heptamelus ochroleucus Stephens = Melicerta ochroleucus Stephens;

17 Halticorcus bhaumiki Basu et Sengupta = Schenklingia bhaumiki Basu and Sengupta;

18 Halticorcus hiranoi Takizawa = Schenklingia hiranoi Takizawa;

19 Halticorcus sauteri Chen = Schenklingia sauteri Chen;

20 Bagous lutulentus Gyllenhal = Bagous glabrirostris var. nigritarsis Thomson;

21 Grypus brunnirostris Fabricius = Curculio Inspectionatus Herbst;

22 Grypus equiseti Fabricius = Grypidius equiseti Fabricius;

Fern miners belong to four orders: Diptera (51 species; 39.8%), Coleoptera (33 species; 25.8%), Lepidoptera (28 species; 21.9%) and Hymenoptera (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, Agromyzidae, Anthomyiidae, Buprestidae, Chrysomelidae and Blasticotomidae 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 Dryopteridaceae (19), Polypodiaceae (18) and Aspleniaceae (15) (Fig. 2; Suppl. material 3). The fern families with the highest numbers of miner species were Dennstaedtiaceae (21), Equisetaceae (21), Polypodiaceae (20) and Aspleniaceae (14) (Fig. 2; Suppl. material 3). With 82 species and 12 families of host ferns and 67 species of fern miners, Polypodiales 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 3.

Linear regressions between (a) the number of host species in each fern family; (b) the number of miner species for each fern family and the total number of fern species in the corresponding family. Families without any host species were not included.

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

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

(3) Hymenoptera: In Tenthredinidae, the genus Heptamelus 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 Heptamelus is involved, except for H. ochroleucus on Athyrium filix-femina (Vikberg 2017). With only 13 species and 3 tribes in Eurasia's temperate region, Blasticotomidae is a small family in the Hymenoptera and their larvae are stem borers on ferns (Taeger et al. 2010, Wikipedia 2019, Santiago-Blay 2004).

(4) Coleoptera: In Buprestidae, both Neotrachys and Endelus have fern-mining habits (Xiao 2018, Bellamy 1997). Most Neotrachys feed on the ferns of Cyatheaceae and Gleicheniaceae (Hespenheide 1980, Hespenheide 1982, Hespenheide 2006). However, some Neotrachys larvae may mine other non-fern plants. For example, N. dominicanus feeds on Arthrostylidium (Poaceae) (Meurgey 2017). The genus Leiopleura is morphologically similar and sometimes confused with Neotrachys, but Leiopleura feeds on Moraceae and Apocynaceae (Hespenheide 1991). Fern-feeding or not could be a clue to distinguish Neotrachys and its related genera. Although there are many publications on Endelus, 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). Equisetaceae has 39 species and eight host species, and Dennstaedtiaceae 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 Equisetaceae and Dennstaedtiaceae that strongly affected the significance of the correlation in Fig. 3b. In particular, the bracken fern (Pteridium aquilinum), one species in Dennstaetiaceae, 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. Dryopteridaceae has 2257 species (Suppl. material 3) and also a cosmopolitan distribution, with many cultivated ornamental species (Olsen and Olsen 2007). Aspleniaceae has 855 species (Suppl. material 3) and also a worldwide distribution (POWO 2019). Polypodiaceae 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 P. aquilinum, Equisetum arvense (Equisetaceae), Athyrium filix-femina (Athyriaceae) and Matteuccia struthiopteris (Onocleaceae) also have a high richness of miners (10, 8 and 6 species, respectively) (Suppl. material 3). The common horsetail (E. arvense) is native throughout the Arctic and temperate regions in the Northern Hemisphere (Schaffner 1930). E. arvense 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 (A. filix-femina) is one of the most abundant fern species in the temperate regions in the Northern Hemisphere (Adam 1995). The ostrich fern (M. struthiopteris) 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.

Acknowledgements

This work was supported by the National Natural Science Foundation of China (31760173 and 41971059) and the Science and Technology Project of Ganzhou City. Kevin Duffy acknowledges the support of the National Research Foundation of South Africa (Grant Numbers 131604). We also thank our colleague, Dr. Zhongyang Li for his significant assistance in our understanding why some fern families host many more miners. Thanks are also given to the two reviewers (Dr. Charles Eiseman and Dr. Yume Imada) for their valuable comments, which significantly improved the manuscript.

References

Supplementary materials

Suppl. material 1: The feeding mode and feeding plant organ of each fern miner 
Authors:  Jie Yang, Xiaohua Dai
Data type:  Feeding habits
Suppl. material 2: The number of fern-miners in each insect family and each insect order 
Authors:  Jie Yang, Xiaohua Dai
Data type:  Number of species
Suppl. material 3: The number of miners on each fern species, each fern family and each fern order 
Authors:  Jie Yang, Xiaohua Dai
Data type:  Number of species