A preliminary world checklist of fern-mining insects

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.


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 , 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 . Fewer miner groups (e.g. gracillariid moths, agromyzid flies and leaf-mining chrysomelids) can utilise over 100 plant families , De Prins and De Prins 2020, Santiago-Blay 2004, Spencer 1990, which are mainly angiosperm families, such as Fagaceae and Myrtaceae .
Ferns (Pteridophyta, including both Lycopodiophyta and Polypodiophyta in the broad sense) are the second largest group of vascular plants, just after angiosperms , 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 andHendrix 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 ) 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 andBrown 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 . 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).

Results
We recorded 128 species and 18 families of fern miners (  Lawton 1982, Lawton 1976, MacGarvin et al. 1986, Rigby and Lawton 1981, Spencer 1990 Agromyzidae  (15)    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 (R = 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 (R = 0.110, t = 1.495, P = 0.152; Fig. 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) 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 . 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.
(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  . Apart from species richness in a fern taxonomic group, the distribution range should also be considered as an important component of 'plant apparency' ). 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 fernmining insects.