A checklist of gymnosperm-feeding leafminers (Arthopoda, Insecta) in North America and Europe

Taibin Chen; Xiaohua Dai; Charles Eiseman

doi:10.3897/BDJ.10.e91313

Biodiversity Data Journal : Research Article

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Research Article

A checklist of gymnosperm-feeding leafminers (Arthopoda, Insecta) in North America and Europe

Taibin Chen^‡, Xiaohua Dai^‡,§,|, Charles Eiseman^¶

‡ Leafminer Group, School of Life Sciences, Gannan Normal University, Ganzhou, China

§ National Navel-Orange Engineering Research Center, Ganzhou, China

| Ganzhou Key Laboratory of Nanling Insect Biology, Ganzhou, China

¶ none, Northfield, MA, United States of America

Corresponding author: Xiaohua Dai (xiaohuadai@gnnu.edu.cn)

Academic editor: Robert Tropek

Received: 06 Aug 2022 | Accepted: 19 Sep 2022 | Published: 28 Sep 2022

This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Citation: Chen T, Dai X, Eiseman C (2022) A checklist of gymnosperm-feeding leafminers (Arthopoda, Insecta) in North America and Europe. Biodiversity Data Journal 10: e91313. https://doi.org/10.3897/BDJ.10.e91313

Abstract

The leafminers on gymnosperms receive much less attention than those on either angiosperms or ferns. Given the distinctly different leaf shape and leaf venation found in gymnosperms, they would be expected to host significantly different leafminer groups. Very few comprehensive reports on gymnosperm-feeding leafminers have been presented.

Based on the well-studied fauna in North America and Europe, we compiled a list of 133 species, 30 genera and 13 families of gymnosperm-feeding leafminers. The gymnosperm-mining families (in descending order of leafminer number) included Tortricidae, Gelechiidae, Argyresthiidae, Yponomeutidae, Batrachedridae, Pyralidae, Adelidae, Agromyzidae, Blastobasidae, Bucculatricidae, Coleophoridae, Curculionidae and Noctuidae. There were 109 species, 22 genera and ten families in North America and 34 species, 19 genera and nine families in Europe. We compiled a list of 102 species and 16 genera of host plants, belonging to four families: Pinaceae, Cupressaceae, Taxaceae and Zamiaceae. There were 84 host species, 15 genera and three host families in North America and 46 host species, ten genera and three host families in Europe. Dominant gymnosperm-mining families and dominant host families were generally the same in the two continents.

Keywords

gymnosperm, leafminer, host plant, Pinaceae, Cupressaceae

Introduction

Leafminers are insects that feed inside plant leaves during some or all larval stages, leaving externally visible feeding trails known as leaf mines (Hering 1951, Hespenheide 1991, Dai et al. 2011, Liu et al. 2015, Dai et al. 2018, Yang et al. 2021, Eiseman 2022, Ellis 2022). There are four orders, over 50 families and over 10000 leafminer species worldwide (Csóka 2003, Hirowatari 2009, Liu et al. 2015). Most leafminers are monophagous or oligophagous and different leaf-mining genera or families often have distinct leaf-mine characteristics, which can be helpful for the identification of leafminers (Sinclair and Hughes 2010, Dai et al. 2011, Liu et al. 2015). Moreover, the long-term persistence of leaf mines on either extant or extinct plants can provide a valuable basis for ecologists and paleoecologists to reconstruct life histories and interspecific relationships (Dai et al. 2018, Yang et al. 2021).

Host plants of leafminers encompass nearly all vascular plant groups, including lycophytes, ferns, gymnosperms and angiosperms (Kristensen and Schmidt-Rhaesa 1998, Yang et al. 2021, Eiseman 2022). Unlike the leaves of other plant groups, those of most gymnosperms are needle-like or scale-like, with small leaf areas (Zhang and Gao 2012, Mou et al. 2016, Jacobsen 2021). In addition, leaf veins of many gymnosperms extend to the leaf tips as parallel straight lines and leaf veins of many angiosperms are present as reticulated structures (Boyce 2005, Nicotra et al. 2011). Furthermore, gymnosperms generally have much lower leaf vein densities than angiosperms (Boyce 2008, Boyce 2009, Brodribb and Feild 2010, Brodribb et al. 2010, Nicotra et al. 2011). Small leaves are less likely to be mined than large leaves (Faeth 1991, Low et al. 2009, Dai et al. 2011) and leaf venation patterns may affect the host plant preference and larval feeding paths of leafminers (Ayabe 2010, Dai et al. 2011). Therefore, the leafminers on gymnosperms should be significantly different from those on either typical ferns or angiosperms. Differences between the leafminer faunas of gymnosperms and angiosperms are likely also strongly influenced by phytochemicals, such as secondary metabolites (SMs) (Hespenheide 1991, Dai et al. 2011). Alkaloids, steroids and phenolic acids are less widely distributed in gymnosperms than in angiosperms , while phenypropanoids, lignin and coumarin are more widely distributed in gymnosperms than in angiosperms (Wang 2006, Zhang 2018, Zhang et al. 2020). However, whether these physical and chemical differences shape distinct leafminer groups on gymnosperms and angiosperms requires further investigation.

Compared to angiosperms and ferns (Godfray 1984, Yang et al. 2021), few comprehensive reports on gymnosperm-feeding leafminers have been presented (Eiseman 2022). Therefore, in this study, we compile a checklist of gymnosperm-feeding leafminers and their host plants in North America and Europe, hoping to provide some valuable information on insect-gymnosperm relationships.

Material and methods

Gymnosperm leafminers and their host plants have been more thoroughly studied in North America and Europe than on other continents (Eiseman 2022, Ellis 2022). The information on names and hosts of gymnosperm-feeding leafminers (Suppl. materials 1, 2) was obtained from the book 'Leafminers of North America' (Eiseman 2022), the websites 'Plant Parasites of Europe' (https://bladmineerders.nl) (Ellis 2022) and 'British Leafminers' (http://www.leafmines.co.uk/index.htm) (Edmunds et al. 2022) and a recent publication on conifer-feeding Batrachedra species (Berggren et al. 2022). The number of species in each gymnosperm family and the scientific names, authorships and publication years for insect species were compiled from the website 'Catalogue of Life' (https://www.catalogueoflife.org/) (Hobern et al. 2021).

Note that the book 'Leafminers of North America' covers only miners that occur in the continental US and Canada (Eiseman 2022), so some species that occur only in Mexico or the Caribbean may be missed. The website 'Plant Parasites of Europe' includes records from ornamental and crop plants, but excludes those from indoor ornamentals, greenhouse plants, uncommon ornamentals, exotics in botanical gardens and cultivars (Ellis 2022). Some host plants have been recorded only at the genus level, especially in the European datasets (Edmunds et al. 2022, Eiseman 2022, Ellis 2022). To be consistent in these cases, we use "spp." after a genus name to indicate one or more unknown host plant species in this genus. However, such cases are uncommon in the above sources.

In our checklist, both non-native leafminers and non-native host plants for the respective biogeographical regions are included. For example, Thuja and Pseudotsuga are not native to Europe, but they were also incorporated into the host plants of European gymnosperm-feeding leafminers and Spilonota laricana, a European moth introduced in North America, is listed for both continents (Eiseman 2022, Ellis 2022). The insect species that feed as leafminers only for part of their larval development (e.g. Coleotechnites carbonaria, C. gibsonella) are also included (Eiseman 2022, Ellis 2022). Insects, whose status as leafminers is uncertain and plants that require confirmation as hosts for a given leafminer, are marked with a question mark (?) before their scientific name in Table 1 and Suppl. materials 1, 2. Such insects and plants are included in the statistics. However, insect species without full scientific names (i.e. undescribed species) and those without definite host records to at least the plant genus level (e.g. Rhyacionia blanchardi, R. pallifasciata, R. salmonicolor and R. versicolor) are excluded (Eiseman 2022). Such cases are uncommon in the above sources.

There are several parasitic modes of gymnosperm-feeding insects, including miner, borer, galler etc. (Brown 2018, Eiseman 2022, Ellis 2022). Species with parasitic modes, other than leaf-mining, were not included in this study, unless they feed as leafminers in early instars. Bark-mining species (e.g. Spulerina corticicola (De Prins and De Prins 2022), Marmara fasciella, M. oregonensis and other undetermined Marmara species (Fitzgerald 1975, Eiseman 2022), were excluded from this study, as were species with unknown parasitic modes.

Results

In total, there were 133 species, 30 genera and 13 families of gymnosperm-feeding leafminers in the two continents, with 109 species, 22 genera and ten families in North America and 34 species, 19 genera and nine families in Europe, with only ten leafminer species occurring in both North America and Europe (Table 1). The leaf-mining families were Tortricidae, Gelechiidae, Argyresthiidae, Yponomeutidae, Batrachedridae, Pyralidae, Adelidae, Agromyzidae, Blastobasidae, Bucculatricidae, Coleophoridae, Curculionidae and Noctuidae (Table 1).

Table 1.

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A checklist of gymnosperm-feeding leafminers in North America and Europe.

Miner family	Miner species	Host plants	Distribution Region
Lepidoptera
Adelidae	Nemophora associatella Zeller, 1839	Abies alba	Europe
Argyresthiidae	Argyresthia abdominalis Zeller, 1839	Juniperus communis	Europe
Argyresthiidae	Argyresthia affinis Braun, 1940	Juniperus virginiana	North America
Argyresthiidae	Argyresthia annettella Busck, 1907	Juniperus communis	North America
Argyresthiidae	Argyresthia arceuthobiella Busck, 1917	Calocedrus decurrens	North America
Argyresthiidae	Argyresthia aureoargentella Brower, 1953	Thuja occidentalis	North America
Argyresthiidae	Argyresthia aurulentella Stainton, 1849	Juniperus communis, Juniperus foetidissima	Europe
Argyresthiidae	Argyresthia canadensis Freeman, 1972	Thuja occidentalis	North America
Argyresthiidae	Argyresthia cupressella Walsingham, 1890	Chamaecyparis spp., Cupressus spp., Juniperus spp., Sequoia sempervirens, Thuja spp.	North America, Europe*
Argyresthiidae	Argyresthia dilectella Zeller, 1874	Chamaecyparis spp., Juniperus communis, Juniperus sabina	Europe
Argyresthiidae	Argyresthia flexilis Freeman, 1960	Pinus flexilis	North America
Argyresthiidae	Argyresthia franciscella Busck, 1915	Cupressus macrocarpa	North America
Argyresthiidae	Argyresthia freyella Walsingham, 1890	Juniperus virginiana	North America
Argyresthiidae	Argyresthia fundella Fischer von Röslerstamm, 1835	Abies alba, Abies balsamea, Abies concolor, Abies grandis, Abies nordmanniana, Abies numidica	Europe
Argyresthiidae	Argyresthia libocedrella Busck, 1917	Calocedrus decurrens, Chamaecyparis lawsoniana	North America
Argyresthiidae	Argyresthia pilatella Braun, 1910	Pinus radiata, ?Pinus torreyana	North America
Argyresthiidae	Argyresthia reticulata Staudinger, 1877	Juniperus communis	Europe
Argyresthiidae	?Argyresthia thoracella Busck, 1907	Juniperus spp.	North America
Argyresthiidae	Argyresthia thuiella Packard, 1871	Chamaecyparis lawsoniana, Cupressus spp.,Thuja occidentalis, Thuja plicata	North America, Europe*
Argyresthiidae	Argyresthia trifasciae Braun, 1910	Cupressus macrocarpa	North America
Argyresthiidae	Argyresthia trifasciata Staudinger, 1871	Chamaecyparis lawsoniana, Cupressus x leylandii, Juniperus chinensis, Juniperus horizontalis, Juniperus sabina, Juniperus squamata, Juniperus virginiana, Juniperus x media, Thuja occidentalis	Europe
Batrachedridae	Batrachedra confusella Berggren, Aarvik, Huemer, Lee et Mutanen, 2022	Pinus sylvestris	Europe
Batrachedridae	Batrachedra pinicolella Zeller, 1839	Abies spp., Picea abies, Picea glauca, Picea pungens, Picea rubens, Pinus spp.	North America*, Europe
Blastobasidae	Blastobasis vittata Wollaston, 1858	Picea spp., Taxus baccata	Europe
Bucculatricidae	Bucculatrix inusitata Braun, 1963	?Juniperus communis	North America
Coleophoridae	Coleophora laricella Hübner, 1817	Larix decidua, Larix gmelinii, Larix kaempferi, Larix laricina, Larix occidentalis, Larix sibirica, Pseudotsuga menziesii	North America*, Europe
Gelechiidae	Chionodes electella Zeller, 1839	Abies alba, Abies pinsapo, Juniperus communis, Picea abies	Europe
Gelechiidae	Chionodes retiniella Barnes & Busck, 1920	Pinus ponderosa, Pinus sabiniana, Tsuga heterophylla	North America
Gelechiidae	Coleotechnites albicostata Freeman, 1965	Juniperus virginiana	North America
Gelechiidae	Coleotechnites apicitripunctella Clemens, 1860	Tsuga canadensis	North America
Gelechiidae	Coleotechnites ardas Freeman, 1960	Pinus contorta var. latifolia	North America
Gelechiidae	Coleotechnites atrupictella Dietz, 1900	Abies balsamea, Abies grandis, Abies lasiocarpa, Picea engelmannii, Picea glauca, Picea mariana, Picea rubens, Picea sitchensis, Pinus ponderosa, Pseudotsuga menziesii, Tsuga heterophylla	North America
Gelechiidae	Coleotechnites biopes Freeman, 1960	Pinus contorta var. latifolia	North America
Gelechiidae	Coleotechnites blastovora McLeod, 1962	Picea glauca	North America
Gelechiidae	Coleotechnites canusella Freeman, 1957	Pinus banksiana, Pinus contorta var. latifolia	North America
Gelechiidae	Coleotechnites carbonaria Freeman, 1965	Juniperus spp.	North America
Gelechiidae	Coleotechnites condignella Busck, 1929	Pinus ponderosa	North America
Gelechiidae	Coleotechnites coniferella Kearfott, 1907	Pinus banksiana	North America
Gelechiidae	Coleotechnites ducharmei Freeman, 1962	Picea glauca, Picea mariana, Picea rubens	North America
Gelechiidae	Coleotechnites edulicola Hodges & Stevens, 1978	Pinus edulis	North America
Gelechiidae	Coleotechnites florae Freeman, 1960	Pinus contorta var. latifolia	North America
Gelechiidae	Coleotechnites gibsonella Kearfott, 1907	Juniperus communis	North America
Gelechiidae	Coleotechnites granti Freeman, 1965	Abies grandis	North America
Gelechiidae	Coleotechnites juniperella Kearfott, 1903	Juniperus communis	North America
Gelechiidae	Coleotechnites laricis Freeman, 1965	Larix laricina	North America
Gelechiidae	Coleotechnites lewisi Freeman, 1960	Pinus flexilis	North America
Gelechiidae	Coleotechnites macleodi Freeman, 1965	Tsuga canadensis	North America
Gelechiidae	Coleotechnites martini Freeman, 1965	Picea abies, Picea glauca	North America
Gelechiidae	Coleotechnites milleri Busck, 1914	Pinus contorta var. murrayana	North America
Gelechiidae	?Coleotechnites moreonella Heinrich, 1920	?Pinus ponderosa, Pinus ponderosa var. scopulorum	North America
Gelechiidae	Coleotechnites obliquistrigella Chambers, 1872	Juniperus virginiana	North America
Gelechiidae	Coleotechnites occidentis Freeman, 1965	Juniperus scopulorum	North America
Gelechiidae	Coleotechnites piceaella Kearfott, 1903	Abies balsamea, Picea abies, Picea glauca, Picea mariana, Picea omorika, Picea pungens, Picea rubens	North America, Europe*
Gelechiidae	Coleotechnites pinella Busck, 1906	Pinus ponderosa	North America
Gelechiidae	Coleotechnites ponderosae Hodges & Stevens, 1978	Pinus ponderosa	North America
Gelechiidae	Coleotechnites resinosae Freeman, 1960	Pinus banksiana, Pinus resinosa	North America
Gelechiidae	Coleotechnites sp.	Pinus jeffreyi	North America
Gelechiidae	Coleotechnites stanfordia Keifer, 1933	Cupressus macrocarpa	North America
Gelechiidae	Coleotechnites starki Freeman, 1957	Pinus contorta var. latifolia	North America
Gelechiidae	Coleotechnites thujaella Kearfott, 1903	Thuja occidentalis	North America
Gelechiidae	?Coleotechnites variiella Chambers, 1872	Taxodium distichum	North America
Gelechiidae	Dichomeris marginella Fabricius, 1781	Juniperus spp.	North America*, Europe
Gelechiidae	Exoteleia anomala Hodges, 1986	Pinus ponderosa	North America
Gelechiidae	Exoteleia burkei Keifer, 1932	Pinus attenuata, Pinus coulteri, Pinus radiata, Pinus sabiniana	North America
Gelechiidae	Exoteleia chillcotti Freeman, 1963	Pinus palustris	North America
Gelechiidae	Exoteleia dodecella Linnaeus, 1758	Larix decidua, Pinus banksiana, Pinus mugo, Pinus nigra, Pinus resinosa, Pinus strobus, Pinus sylvestris, Pinus uncinata	North America*, Europe
Gelechiidae	Exoteleia nepheos Freeman, 1967	Pinus mugo, Pinus resinosa, Pinus sylvestris	North America
Gelechiidae	Exoteleia pinifoliella Chambers, 1880	Pinus banksiana, Pinus echinata, Pinus palustris, Pinus pungens, Pinus resinosa, Pinus rigida, Pinus sylvestris, Pinus taeda, Pinus virginiana, ?Pinus contorta, ?Pinus ponderosa	North America
Noctuidae	Feralia jocosa Guenée, 1852	Abies balsamea, Abies grandis, Abies lasiocarpa, Larix laricina, Larix occidentalis, Picea mariana, Picea engelmannii, Picea glauca, Picea sitchensis, Pseudotsuga menziesii, Tsuga canadensis, Tsuga heterophylla, Tsuga mertensiana	North America
Pyralidae	Dioryctria reniculelloides Mutuura & Munroe, 1973	Abies spp., Larix spp., Picea engelmannii, Picea glauca, Picea mariana, Picea pungens, Picea sitchensis, ?Picea rubens, ?Pinus contorta, Pseudotsuga menziesii, Tsuga heterophylla	North America
Pyralidae	Pococera robustella Zeller, 1848	Pinus banksiana, Pinus echinata, Pinus elliottii, Pinus mugo, Pinus palustris, Pinus resinosa, Pinus rigida, Pinus strobus, Pinus sylvestris, Pinus taeda, Pinus virginiana	North America
Tortricidae	Aethes rutilana Hübner, 1817	Juniperus spp.	North America
Tortricidae	Archips oporana Linnaeus, 1758	Abies alba, Juniperus communis, Larix decidua, Picea abies, Pinus sylvestris, Thuja occidentalis	Europe
Tortricidae	Archips packardiana Fernald, 1886	Abies amabilis, Abies balsamea, Abies lasiocarpa, Larix spp., Picea abies, Picea engelmannii, Picea glauca, Picea mariana, Picea pungens, Picea rubens, Picea sitchensis, Pinus banksiana, Pinus contorta, Tsuga canadensis, Tsuga heterophylla	North America
Tortricidae	Argyrotaenia occultana Freeman, 1942	Abies balsamea, Larix laricina, Picea engelmannii, Picea glauca, Picea mariana, Picea rubens, Pinus contorta, Pseudotsuga menziesii, Tsuga spp.	North America
Tortricidae	Argyrotaenia pinatubana Kearfott, 1905	Pinus strobus	North America
Tortricidae	Argyrotaenia tabulana Freeman, 1944	Pinus albicaulis, Pinus banksiana, Pinus contorta var. latifolia, Pinus ponderosa	North America
Tortricidae	Choristoneura carnana Barnes & Busck, 1920	Abies concolor, Pseudotsuga macrocarpa, Pseudotsuga menziesii	North America
Tortricidae	Choristoneura fumiferana Clemens, 1865	Abies balsamea, Larix laricina, Picea glauca, Picea rubens, Pinus spp.	North America
Tortricidae	Choristoneura houstonana Grote, 1873	Juniperus ashei, Juniperus californica, Juniperus chinensis, Juniperus scopulorum, Juniperus virginiana, ?Juniperus occidentalis, ?Juniperus osteosperma, Juniperus virginiana	North America
Tortricidae	Choristoneura lambertiana Busck, 1915	Abies spp., Pinus spp.	North America
Tortricidae	Choristoneura occidentalis Freeman, 1967	Abies spp., Picea spp.	North America
Tortricidae	Choristoneura orae Freeman, 1967	Abies amabilis, Picea sitchensis	North America
Tortricidae	Choristoneura pinus Freeman, 1953	Pinus spp.	North America
Tortricidae	Choristoneura retiniana Walsingham, 1879	Abies concolor, Abies grandis, Abies magnifica	North America
Tortricidae	Choristoneura spaldingana Obraztsov, 1962	Abies concolor	North America
Tortricidae	Clavigesta purdeyi Durrant, 1911	Pinus contorta, Pinus nigra, Pinus sylvestris	Europe
Tortricidae	Cymolomia hartigiana Ratzeburg, 1840	Abies alba, Picea abies	Europe
Tortricidae	Dichelia histrionana Frölich, 1828	Abies alba, Picea abies	Europe
Tortricidae	Epinotia aridos Freeman, 1960	Pinus contorta var. latifolia	North America
Tortricidae	Epinotia balsameae Freeman, 1965	Abies balsamea	North America
Tortricidae	Epinotia fraternana Haworth, 1811	Abies alba, Abies cephalonica, Abies grandis, Abies nordmanniana	Europe
Tortricidae	Epinotia hopkinsana Kearfott, 1907	Picea sitchensis, Pinus spp.	North America
Tortricidae	Epinotia meritana Heinrich, 1923	Abies concolor, Abies magnifica	North America
Tortricidae	Epinotia nanana Treitschke, 1835	Abies alba, Picea abies, Picea glauca, Picea mariana, Picea pungens, Picea rubens, Picea sitchensis	North America*, Europe
Tortricidae	Epinotia normanana Kearfott, 1907	Picea abies, Picea glauca, Picea pungens, Picea rubens	North America
Tortricidae	Epinotia pusillana Peyerimhoff, 1863	Abies alba	Europe
Tortricidae	Epinotia pygmaeana Hübner, 1799	Abies alba, Picea abies, Picea sitchensis	Europe
Tortricidae	Epinotia subsequana Haworth, 1811	Abies alba, Abies grandis, Picea abies	Europe
Tortricidae	Epinotia tedella Clerck, 1759	Picea abies	Europe
Tortricidae	Epinotia trossulana Walsingham, 1879	Abies concolor, Abies magnifica, ?Pseudotsuga menziesii	North America
Tortricidae	Epinotia tsugana Freeman, 1967	Abies amabilis, Picea sitchensis, Tsuga heterophylla, Tsuga mertensiana	North America
Tortricidae	Pseudohermenias abietana Fabricius, 1787	Abies alba, Picea abies	Europe
Tortricidae	Rhyacionia adana Heinrich, 1923	Pinus banksiana, Pinus resinosa, Pinus sylvestris	North America
Tortricidae	?Rhyacionia aktita Miller, 1978	Pinus elliottii, Pinus rigida, Pinus taeda	North America
Tortricidae	Rhyacionia buoliana Denis & Schiffermüller, 1775	Pinus banksiana, Pinus densiflora, Pinus mugo, Pinus nigra, Pinus palustris, Pinus ponderosa, Pinus resinosa, Pinus rigida, Pinus strobus, Pinus sylvestris, Pinus thunbergii, Pinus virginiana	North America
Tortricidae	?Rhyacionia busckana Heinrich, 1923	Pinus ponderosa, Pinus resinosa, Pinus sylvestris	North America
Tortricidae	?Rhyacionia bushnelli Busck, 1914	Pinus banksiana, Pinus nigra, Pinus ponderosa, Pinus resinosa, Pinus sylvestris	North America
Tortricidae	Rhyacionia frustrana Comstock, 1880	Pinus echinata, Pinus elliottii, Pinus palustris, Pinus ponderosa, Pinus radiata, Pinus resinosa, Pinus rigida, Pinus strobus, Pinus sylvestris, Pinus taeda, Pinus virginiana	North America
Tortricidae	?Rhyacionia fumosana Powell & Miller, 1978	Pinus ponderosa	North America
Tortricidae	?Rhyacionia granti Miller, 1985	Pinus banksiana	North America
Tortricidae	?Rhyacionia jenningsi Powell, 1978	Pinus ponderosa	North America
Tortricidae	?Rhyacionia martinana Powell, 1978	?Pinus edulis	North America
Tortricidae	?Rhyacionia monophylliana Kearfott, 1907	Pinus monophylla	North America
Tortricidae	?Rhyacionia multilineata Powell, 1978	Pinus ponderosa	North America
Tortricidae	?Rhyacionia neomexicana Dyar, 1903	Pinus ponderosa	North America
Tortricidae	?Rhyacionia pasadenana Kearfott, 1907	Pinus contorta, Pinus muricata, Pinus radiata	North America
Tortricidae	?Rhyacionia rigidana Fernald, 1880	Pinus echinata, Pinus resinosa, Pinus rigida, Pinus taeda, Pinus virginiana	North America
Tortricidae	?Rhyacionia sonia Miller, 1967	Pinus banksiana	North America
Tortricidae	?Rhyacionia subcervinana Walsingham, 1879	Pinus jeffreyi, Pinus ponderosa	North America
Tortricidae	?Rhyacionia subtropica Miller, 1961	Pinus elliottii, Pinus palustris, Pinus taeda	North America
Tortricidae	?Rhyacionia zozana Kearfott, 1907	Pinus contorta, Pinus jeffreyi, Pinus ponderosa	North America
Tortricidae	Spilonota laricana Heinemann, 1863	Larix aricina, Larix decidua, Larix kaempferi, Picea sitchensis	North America*, Europe
Tortricidae	Taniva albolineana Kearfott, 1907	Picea abies, Picea engelmannii, Picea glauca, Picea mariana, Picea pungens, Picea rubens, Picea sitchensis	North America
Yponomeutidae	Cedestis gysseleniella Zeller, 1830	Pinus contorta, Pinus mugo, Pinus nigra, Pinus nigra subsp. Laricio, Pinus sylvestris	Europe
Yponomeutidae	Cedestis subfasciella Stephens, 1834	Pinus mugo, Pinus nigra, Pinus sylvestris, Pinus uncinata	Europe
Yponomeutidae	Ocnerostoma friesei Svensson, 1966	Pinus mugo, Pinus sylvestris	Europe
Yponomeutidae	Ocnerostoma piniariella Zeller, 1847	Pinus cembra, Pinus contorta var. latifolia, Pinus monticola, Pinus mugo, Pinus resinosa, Pinus strobus, Pinus sylvestris	North America*, Europe
Yponomeutidae	Ocnerostoma sp.	Pinus resinosa	North America
Yponomeutidae	Ocnerostoma strobivorum Freeman, 1960	Pinus strobus	North America
Yponomeutidae	Zelleria haimbachi Busck, 1915	Pinus arizonica, Pinus attenuata, Pinus banksiana, Pinus contorta, Pinus coulteri, Pinus echinata, Pinus engelmannii, Pinus jeffreyi, Pinus muricata, Pinus ponderosa, Pinus radiata, Pinus resinosa, Pinus sylvestris, Pinus taeda	North America
Diptera
Agromyzidae	Liriomyza schmidti Aldrich, 1929	?Zamia integrifolia	North America
Coleoptera
Curculionidae	Brachonyx pineti Paykull, 1792	Pinus sylvestris, Pinus uncinata	Europe

Note: Detailed information such as insect taxonomy, host taxonomy and local distribution are provided in Suppl. materials 1, 2. An asterisk marking the name of a continent (e.g. Europe*) indicates that the corresponding herbivore species is introduced in that region. A question mark "?" before an insect name indicates that this species has not been confirmed as a leafminer and a question mark "?" before a plant name indicates that its status as a host of the corresponding insect species requires confirmation.

In Tortricidae, there were 53 species and 12 genera of gymnosperm-feeding leafminers with 64 host plant species and nine host genera, including 43 leafminer species with 58 host species, eight host genera and two host families in North America and 12 leafminer species with 13 host species, six host genera and two host families in Europe (Table 2). Amongst tortricid genera, Rhyacionia and EpinotiaEpinotia Epinotia were the two richest in gymnosperm-feeding leafminer species. There were 19 leafminer species and 21 host species in Rhyacionia and 13 leafminer species and 19 host species in Epinotia. Whereas EpinotiaEpinotia Epinotia was recorded in both North America and Europe, Rhyacionia was recorded only in North America. Amongst tortricid species, Archips packardiana, with 15 host species, was the leafminer with the most host species and was recorded only in North America (Table 1). Archips oporana, with six host species, was the leafminer with the second most host species and was recorded only in Europe (Table 1).

Table 2.

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Number of gymnosperm-feeding leafminer species and number of host plant species used by these insects, in different leafminer families in North America (NA) and Europe (EU).

Leafminer order

Leafminer family

Number of leafminer species in each leafminer family

Number of host species in each leafminer family

Leafminer genus

Number of leafminer species in each leafminer genus

Number of host species in each leafminer genus

Lepidoptera

Tortricidae

(NA: 43, EU: 12)

(NA: 58, EU: 13)

Rhyacionia

(NA: 19, EU: 0)

(NA: 21, EU: 0)

Epinotia

(NA: 8, EU: 6)

(NA: 15, EU: 6)

Choristoneura

(NA: 9, EU: 0)

(NA: 22, EU: 0)

Argyrotaenia

(NA: 3, EU: 0)

(NA: 14, EU: 0)

Archips

(NA: 1, EU: 1)

(NA: 15, EU: 6)

Taniva

(NA: 1, EU: 0)

(NA: 7, EU: 0)

Spilonota

(NA: 1, EU: 1)

(NA: 2, EU: 3)

Pseudohermenias

(NA: 0, EU: 1)

(NA: 0, EU: 2)

Dichelia

(NA: 0, EU: 1)

(NA: 0, EU: 2)

Cymolomia

(NA: 0, EU: 1)

(NA: 0, EU: 2)

Clavigesta

(NA: 0, EU: 1)

(NA: 0, EU: 3)

Aethes

(NA: 1, EU: 0)

Gelechiidae

(NA: 41, EU: 4)

(NA: 45, EU: 10)

Coleotechnites

(NA: 33, EU: 1)

(NA: 30, EU: 2)

Exoteleia

(NA: 6, EU: 1)

(NA: 18, EU: 4)

Chionodes

(NA: 1, EU: 1)

(NA: 3, EU: 4)

Dichomeris

(NA: 1, EU: 1)

Argyresthiidae

(NA: 14, EU: 8)

(NA: 13, EU: 22)

Argyresthia

(NA: 14, EU: 8)

(NA: 13, EU: 22)

Yponomeutidae

(NA: 4, EU: 4)

(NA: 17, EU: 7)

Ocnerostoma

(NA: 3, EU: 2)

(NA: 4, EU: 3)

Cedestis

(NA: 0, EU: 2)

(NA: 0, EU: 6)

Zelleria

(NA: 1, EU: 0)

(NA: 14, EU: 0)

Batrachedridae

(NA: 1, EU: 2)

(NA: 4, EU: 4)

Batrachedra

(NA: 1, EU: 2)

(NA: 4, EU: 4)

Pyralidae

(NA: 2, EU: 0)

(NA: 22, EU: 0)

Dioryctria

(NA: 1, EU: 0)

(NA: 11, EU: 0)

Pococera

(NA: 1, EU: 0)

(NA: 11, EU: 0)

Coleophoridae

(NA: 1, EU: 1)

(NA: 6, EU: 7)

Coleophora

(NA: 1, EU: 1)

(NA: 6, EU: 7)

Noctuidae

(NA: 1, EU: 0)

(NA: 13, EU: 0)

Feralia

(NA: 1, EU: 0)

(NA: 13, EU: 0)

Blastobasidae

(NA: 0, EU: 1)

(NA: 0, EU: 2)

Blastobasis

(NA: 0, EU: 1)

(NA: 0, EU: 2)

Adelidae

(NA: 0, EU: 1)

Nemophora

(NA: 0, EU: 1)

Bucculatricidae

(NA: 1, EU: 0)

Bucculatrix

(NA: 1, EU: 0)

Diptera

Agromyzidae

(NA: 1, EU: 0)

Liriomyza

(NA: 1, EU: 0)

Coleoptera

Curculionidae

(NA: 0, EU: 1)

(NA: 0, EU: 2)

Brachonyx

(NA: 0, EU: 1)

(NA: 0, EU: 2)

In Gelechiidae, there were 42 species and four genera of gymnosperm-feeding leafminers with 50 host plant species and ten host genera, including 41 leafminer species with 45 host species, ten host genera and two host families in North America and four leafminer species with ten host species, five host genera and two host families in Europe (Table 2). Amongst gelechiid genera, Coleotechnites is the richest in gymnosperm-feeding leafminer species, with 33 leafminer species in North America, but only one species in Europe.

In Argyresthiidae, there were 20 species and one genus of gymnosperm-feeding leafminers with 28 host plant species and eight host genera, including 14 leafminer species with 13 host species, seven host genera and two host families in North America and eight leafminer species with 22 host species, five host genera and two host families in Europe (Table 2). All of these insects belong to the genus Argyresthia (Table 2).

In Yponomeutidae, there were seven species and three genera of gymnosperm-feeding leafminers with 22 host plant species and one host genus, including four leafminer species with 17 host species, one host genus and one host family in North America and four leafminer species with seven host species, one host genus and one host family in Europe (Table 2). Amongst yponomeutid genera, Ocnerostoma is the richest in gymnosperm-feeding leafminer species, with four leafminer species and seven host species.

Of all these leafminers, just one polyphagous species (Liriomyza schmidti) is presumed to feed on both gymnosperms and angiosperms and it is also the only gymnosperm-mining dipteran fly in our study. The other 132 species (i.e. > 99%) feed exclusively on gymnosperms.

For host plants, there were 102 species, 16 genera and four families represented in the two continents. Eighty-four species, 15 genera and three families were found in North America, including Pinaceae, Cupressaceae and Zamiaceae (Table 3). Forty-six species, ten genera and three families were found in Europe, including Pinaceae, Cupressaceae and Taxaceae (Table 3).

Table 3.

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XLSX

Number of host species and associated leafminer species in different gymnosperm plant families in North America (NA) and Europe (EU).

Gymnosperm family

Number of host species in each gymnosperm family

Number of leafminers in each gymnosperm family

Gymnosperm genus

Number of host species in each gymnosperm genus

Number of leafminers in each gymnosperm genus

Pinaceae

(NA: 65, EU: 29)

102

(NA: 83, EU: 26)

Pinus

(NA: 35, EU: 8)

(NA: 59, EU: 10)

Abies

(NA: 7, EU:9)

(NA: 18, EU:13)

Picea

(NA: 9, EU: 5)

(NA: 18, EU: 13)

Larix

(NA: 8, EU: 6)

(NA: 8, EU: 4)

Tsuga

(NA: 4, EU: 0)

(NA: 9, EU: 0)

Pseudotsuga

(NA: 2, EU: 1)

(NA: 6, EU: 1)

Cupressaceae

(NA: 18, EU: 16)

(NA: 25, EU: 10)

Juniperus

(NA: 9, EU: 9)

(NA: 15, EU: 9)

Cupressus

(NA: 1, EU: 2)

(NA: 4, EU: 3)

Thuja

(NA: 2, EU: 3)

(NA: 5, EU: 4)

Chamaecyparis

(NA: 2, EU: 2)

(NA: 2, EU: 4)

Calocedrus

(NA: 1, EU: 0)

(NA: 2, EU: 0)

Sequoia

(NA: 1, EU: 0)

Taxodium

(NA: 1, EU: 0)

Platycladus

(NA: 1, EU: 0)

Taxaceae

(NA: 0, EU: 1)

Taxus

(NA: 0, EU: 1)

Zamiaceae

(NA: 1, EU: 0)

Zamia

(NA: 1, EU:0)

(NA: 1, EU: 0)

In Pinaceae, there were 74 host species, six host genera and 102 associated leafminer species, including 65 host species, six host genera and 83 leafminer species in North America and 29 host species, five host genera and 26 leafminer species in Europe (Table 3). Amongst gymnosperm genera, Pinus was richest in both host species and leafminer species, with 38 host species and 67 leafminer species, including 35 host species and 59 leafminer species in North America and eight host species and ten leafminer species in Europe.

In Cupressaceae, there were 26 host species, eight host genera and 32 associated leafminer species, including 18 host species, eight host genera and 25 leafminer species in North America and 16 host species, four host genera and ten leafminer species in Europe (Table 3). Amongst gymnosperm genera, Juniperus was second richest in host species and fourth richest in leafminer species, with 14 host species and 22 leafminer species, including nine host species and 15 leafminer species in North America and nine host species and nine leafminer species in Europe (Table 3) .

In North America, gymnosperm-feeding leafminers belong to ten families, mostly in Tortricidae (43 species, 39.45%), Gelechiidae (41 species, 37.61%), Argyresthiidae (14 species, 12.84%), Yponomeutidae (four species, 3.67%) and Pyralidae (two species, 1.83%) (Table 2, Fig. 1a). In Europe, gymnosperm-feeding leafminers belong to nine families, mostly in Tortricidae (12 species, 35.29%), Argyresthiidae (eight species, 23.53%), Gelechiidae (four species, 11.76%), Yponomeutidae (four species, 11.76%) and Batrachedridae (two species, 5.88%) (Table 2, Fig. 1b).

Figure 1.

Percentage distribution of the gymnosperm-mining species in different insect families.

a: North America
b: Europe

There were two orders and two classes of host plants for gymnosperm-feeding leafminers in the two continents, including the orders of Pinales (class Pinopsida) and Cycadales (class Cycadopsida) (Table 3). Almost all host plants belong to the order Pinales, with just one belonging to the order Cycadales (Table 3).

In North America, there were three families and two orders of host plants, including Pinales (Pinaceae and Cupressaceae) and Cycadales (Zamiaceae) (Table 3). In Europe, there were three families of host plants, all belonging to the order Pinales, including Pinaceae, Cupressaceae and Taxaceae (Table 3). Pinaceae had the largest number of host species in both North America and Europe, but with different genera having the most host species. In North America, the genus Pinus (35 host species) of Pinaceae had the most host species (Table 3), while the genera Abies (nine host species) of Pinaceae and Juniperus (nine host species) of Cupressaceae had the most host species in Europe (Table 3).

Discussion

In this paper, we provide a list of the known gymnosperm-feeding leafminers and their host plants in North America and Europe. Here, we give a brief overiew of gymnosperm-mining families in the two continents, in descending order of species richness:

(1) Tortricidae (junior synonym: Olethreutidae) (Lepidoptera). Insects within this family are able to feed on many plant parts, usually as leaf-rollers or borers, with some inducing galls (Brown 2018, Eiseman 2022, Ellis 2022). Only a few tortricid species have mining behaviour (Ellis 2022). Most of these are not typical leafminers, with the mining behaviour occurring only in early instars and older larvae feed as borers in other plant parts or externally in leaf shelters (Eiseman 2022, Ellis 2022). It should be noted here that species of Rhyacionia, which we have reported to be the tortricid genus richest in gymnosperm leaf-mining species, feed primarily as shoot borers. The few Rhyacionia species for which detailed life history information is available all feed initially as leafminers and the rest are only assumed to do so (Eiseman 2022). On the other hand, several Epinotia species do mine in leaves of Pinaceae throughout their development (Eiseman 2022). Many tortricid species are conifer-feeding specialists (Brown 2018). For example, the leaf-mining species Choristoneura fumiferana feeds exclusively on Pinaceae (Eiseman 2022) and is an important pest of coniferous forest trees in North America (Brown 2018). The number of leafminer species in this family was greatest amongst all mining families of gymnosperms in both North America and Europe (Table 2).

(2) Gelechiidae (Lepidoptera). Host plants of this family are extremely diverse, with more than 80 host families utilised (Kristensen and Schmidt-Rhaesa 1998). Only a small proportion of gelechiid species have mining behaviour (Kristensen and Schmidt-Rhaesa 1998) and, as with Tortricidae, many of them do so only in early instars (Eiseman 2022). The larvae of several gelechiid genera feed on gymnosperms and three of these (Coleotechnites, Exoteleia and Chionodes) include species that feed exclusively on Pinaceae (Brown 2018). One needle-mining Coleotechnites species was first observed on Pinus jeffreyi in southern California in 1963, but remains undescribed (Luck 1976, Eiseman 2022).

(3) Argyresthiidae (Lepidoptera). This family includes about 160 species worldwide (Eiseman 2022). The larvae usually feed on host plants as miners or as borers in buds, flowers, seeds, fruit, cones or twigs (Eiseman 2022). In total, 42% of species feed on conifers as leafminers (Powell 1980, Brown 2018). Over 13 families of plants are utilised by larvae of the genus Argyresthia (gymnosperms and dicots) (Kristensen and Schmidt-Rhaesa 1998). However, there is no record of larvae of this genus feeding on angiosperms as leafminers, with the exception of an erroneous report of the willow-feeding species A. pygmaeella doing so (it is in fact a shoot- and catkin-borer) (Eiseman 2022).

(4) Yponomeutidae (Lepidoptera). At least 18 plant families are utilised by yponomeutid moths, including gymnosperms (Pinaceae) and angiosperms (e.g. Betulaceae, Celastraceae and Rosaceae) (Ulenberg 2009). Most yponomeutid species are external feeders on leaves (Kristensen and Schmidt-Rhaesa 1998) and only a few are leafminers (Eiseman 2022). The larvae of three yponomeutid genera feed on gymnosperms (Eiseman 2022, Ellis 2022). Amongst the pine needle-mining Ocnerostoma species is one that feeds on Pinus resinosa and remains undescribed (Freeman 1960, Maier et al. 2011). Zelleria haimbachi is another Pinus-mining specialist (Brown 2018, Eiseman 2022); when nearly mature, the larvae move more freely and web around the needle bases (Eiseman 2022).

(5) Batrachedridae (Lepidoptera). This is a small family of tiny moths, with only a few species feeding as leafminers (Ellis 2022). In North America, just two species are known to feed as leafminers (Batrachedra concitata on Agave and B. pinicolella on Abies) (Eiseman 2022). Two gymnosperm-mining batrachedrid species occur in Europe and one of these (B. pinicolella) has recently invaded North Amercia (Maier 2005, Berggren et al. 2022).

(6) Pyralidae (Lepidoptera). The larvae of pyralid moths have diverse types of feeding behaviour. Some act as leaf-tiers or leaf-rollers, others as borers in stems, cambium or fruit and still others even feed on dead plant material (Eiseman 2022, Ellis 2022). Only a few pyralid species are leafminers, with very few feeding on gymnosperms (Eiseman 2022, Ellis 2022). In North America and Europe, just two species are gymnosperm-feeding leafminers (Pococera robustella and Dioryctria reniculelloides), with both mining leaves only in early instars (Eiseman 2022, Ellis 2022).

(7) Adelidae (Lepidoptera). This is a small and relatively primitive family (Kozlov and Robinson 1996) with about 350 species (Hobern et al. 2021). Many adelid species are leafminers in their early instars (Kozlov and Robinson 1996). Just one species (Nemophora associatella) is recorded as an Abies-feeding leafminer in Europe (Ellis 2022).

(8) Agromyzidae (Diptera). This is a family widely distributed throughout the world (Mujica and Kroschel 2011) and it is one of the largest fly families (Civelek 2003, Dousti 2010). It is well-known for diverse leafminers, some of which are economically important (Benavent-Corai et al. 2005). About half of agromyzid species are leafminers (Ellis 2022). The genus Liriomyza alone has more than 300 leaf-mining species (Mujica and Kroschel 2011). More than ten agromyzid genera have mining behaviour in North America alone, but just one species is known to be a gymnosperm-feeding leafminer (Eiseman 2022). Liriomyza schmidti is an extremely polyphagous species with reported hosts in nearly 30 families, one of which is the cycad family Zamiaceae (Eiseman 2022). No agromyzid species is recorded as a gymnosperm-feeding leafminer in Europe (Ellis 2022).

(9) Blastobasidae (Lepidoptera). This is a relatively small moth family with a wide distribution around the world (Karsholt and Sinev 2004, Ellis 2022). Most blastobasid larvae are detritus feeders (Ellis 2022). Conifer-feeding blastobasids are cone feeders or external webbers (Brown 2018) and there are six pine-feeding specialists in the genus Holcocera (Brown 2018). Just one blastobasid species (Blastobasis vittata) is a gymnosperm leafminer in Europe, occasionally mining in yew (Taxus baccata) or spruce (Picea sp.) as young larvae (Ellis 2022).

(10) Bucculatricidae (Lepidoptera). This family has a wide distribution around the world (Vargas and Mundaca 2016, Tokár and Laštůvka 2018). Most bucculatricid species are leafminers in their early instars, while a few species are gallers (Vargas and Mundaca 2016). Bucculatrix inusitata is reportedly a Cupressaceae specialist (Brown 2018), but this is based on a single specimen that is labelled as having been reared from a larva on Juniperus (Braun 1963). This host record requires confirmation, since Bucculatrix larvae commonly wander from their food plants before spinning cocoons and B. inusitata belongs to a group of species that otherwise are virtually all Asteraceae specialists (Braun 1963). No other Bucculatricidae have been reported from gymnosperms in North America or Europe (Eiseman 2022, Ellis 2022).

(11) Coleophoridae (Lepidoptera). Virtually all coleophorid larvae begin their lives as leafminers or within ovules and seeds and, at later larval stages, live in portable silk cases, from which the leaf-mining species continue to make fleck mines (Eiseman 2022, Ellis 2022). In North America and Europe, there is just one gymnosperm-mining species (Coleophora laricella), which is native to Europe and was introduced in North America in the 1800s (Eiseman 2022, Ellis 2022).

(12) Curculionidae (Coleoptera). This family has a wide distribution around the world (Wikipedia 2022) and it is the largest beetle family (Bandeira et al. 2021), but only a small proportion of curculionid species are leafminers (Ellis 2022). Thirty-one species and eight genera in Curculionidae are leafminers in North America, none of them feeding on gymnosperms (Eiseman 2022). However, one curculionid species (Brachonyx pineti) has been recorded as a gymnosperm-feeding leafminer in Europe (Ellis 2022).

(13) Noctuidae (Lepidoptera). This is amongst the largest moth families (Ellis 2022). Many noctuid larvae are external feeders or borers in either stems or roots (Eiseman 2022, Ellis 2022), while only several species have mining behaviour (Eiseman 2022). First instars of a single North American species (Feralia jocosa) have been observed to mine into Tsuga needles, although they do not fully enter the needles as with typical miners (Eiseman 2022). No noctuid species mine gymnosperms in Europe (Ellis 2022).

In both North America and Europe, leafminer groups on angiosperms are extraordinarily diverse, followed by those on gymnosperms, while those on ferns and their allies are the least (Suppl. material 3; Yang et al. 2021, Eiseman 2022, Ellis 2022). Amongst the leafminers on either ferns or angiosperms, Lepidoptera has the most leaf-mining families (Yang et al. 2021, Eiseman 2022, Ellis 2022). Similarly, 11 of the 13 gymnosperm-feeding families belong to Lepidoptera (Table 2). In contrast with angiosperms and ferns, gymnosperms host just one leaf-mining beetle (Coleoptera), one leaf-mining fly (Diptera) and no leaf-mining sawfly (Hymenoptera) species (Table 1). Several leafminer families such as Noctuidae, Curculionidae and Agromyzidae occur in all three vascular plant groups (Yang et al. 2021, Eiseman 2022, Ellis 2022). Agromyzidae is a family best known as leafminers (Spencer 1990). Curculionidae has many leafminer species, but Noctuidae has only a few (Eiseman 2022). Whereas ferns and angiosperms host many specialised leafmining families (e.g. Gracillariidae, Agromyzidae, Anthomyiidae, Tischeriidae, Acanthopteroctetidae, Nepticulidae, Heliozelidae, Bedelliidae, Lyonetiidae, Elachistidae) (Kristensen and Schmidt-Rhaesa 1998, Yang et al. 2021, Eiseman 2022), virtually none of the leafminers of gymnosperms belongs to specialised leafmining families, with the exception of a single extremely polyphagous agromyzid that is believed to be responsible for mines found on Cycadales. It is worth mentioning that, although there are no leafmining gracillariid species on gymnosperms in North America or Europe, there are bark-miners in the genus Marmara (e.g. M. fasciella and M. oregonensis) (Eiseman 2022). However, the focus of this study is on leaf-mining species.

Some insect families, known for their leafmining habits, are absent or rare on gymnosperms (e.g. Tischeriidae, Nepticulidae, Gracillariidae and Agromyzidae). Worldwide, no species of Tischeriidae (Kristensen and Schmidt-Rhaesa 1998, Xu et al. 2021, Alipanah et al. 2022) or Nepticulidae (Powell 1980, Kristensen and Schmidt-Rhaesa 1998, Menken et al. 2009, Doorenweerd et al. 2015) are recorded as leafminers on gymnosperms; both families occur only on angiosperms. In Gracillariidae, although most larvae are leafminers (at least during their early instars) (Eiseman 2022, Ellis 2022), no gracillariid leafminer is recorded on gymnosperms in either North America or Europe (Suppl. material 3; Eiseman 2022, Ellis 2022). However, two gracillariid leafminers are known to feed on gymnosperms in other regions (see below) (Liu et al. 2018, De Prins and De Prins 2022). Agromyzidae, another well-known leafmining family, has many leafminer species on angiosperms, ferns and even bryophytes, but only Liriomyza schmidti is recorded from a gymnosperm and this association has yet to be confirmed by rearing (Spencer 1990, Yang et al. 2021, Eiseman 2022, Ellis 2022).

Generally, North America is richer in gymnosperm leafminers than Europe (species 109:34; genus 22:19; family 10:9) (Table 2). The higher diversity of leafminers found in North America is probably correlated with higher availability of potential host plants. North America has a larger species number and distribution area of gymnosperm hosts than Europe (Fragnière et al. 2015). For example, cycads exist in the Rocky Mountain and Caribbean regions in North America, but not in Europe (Fragnière et al. 2015). In North America, gnetophytes are distributed in the Caribbean regions, Mexico and the vast regions of the US, while in Europe, there are just a few distributed near the southern coast (Fragnière et al. 2015). Although conifers occur in almost all regions of North America (ca. 330 species) and Europe (ca. 100 species), their species number and distribution area in North America is larger (Flora of North America Editorial Committee 1993, Euro+Med 2006, Fragnière et al. 2015).

Leaf-mining insects are greatly affected by leaf features of host plants, including leaf size, leaf thickness, leaf venation and leaf phytochemicals (Hespenheide 1991, Dai et al. 2011). Differences in these features may explain why gymnosperms and angiosperms have significantly different leafminer species. On the other hand, gymnosperms with leaf features similar to those of angiosperms may have correspondingly similar leafminer groups. Gnetum (Gymnospermae: Gnetaceae) is a representative example, with a leaf type closely approximate to that of angiosperms (Spencer 1990, Stewart et al. 1993). Therefore, it is a suitable host candidate for Agromyzidae (Spencer 1990), which is a common leafminer family on angiosperms. Cycads likewise share some herbivorous insect species with angiosperms (Whitaker and Salzman 2020). The palm-like leaves of the cycad Zamia integrifolia (Zamiaceae) might explain why it is an acceptable host for the polyphagous species Liriomyza schmidti, which otherwise is only known to feed on angiosperms (Eiseman 2022). Gracillariidae is a well-known leafminer family, but just two species have been found to feed in leaves of gymnosperms (the Japanese Phyllocnistis podocarpa mines in Podocarpus macrophyllus (Podocarpaceae) and in New Zealand Parectopa leucocyma mines in Agathis australis (Araucariaceae)) (Liu et al. 2018, De Prins and De Prins 2022). This may also be related to the unusual leaf morphology of the host plants. Unlike most conifer species with leaves in the form of scales or needles, podocarps have larger, bilaterally flattened leaves and vein reticulation (Brodribb 2011). Similarly, compared with other typical gymnosperms, the leaves of the genus Agathis are more broad and flattened with rounded tips (Stockey 1982). Therefore, the distinctive leaf structure of host plants may cause the gracillariid leafminers to mine selectively on gymnosperms. Podocarpaceae and Araucariaceae are sister families (Quinn et al. 2002), implying that plant phylogeny and phytochemistry might also play a role in determining the presence/absence of leafminers on plants.

Acknowledgements

This study was financially supported by the National Natural Science Foundation of China (41971059, 32260282, and 31760173), and the Science and Technology Project of Ganzhou City ([2020]60). We thank Dr. Robert Tropek, Dr. John Brown and two anonymous reviewers for valuable suggestions, which have significantly improved the first version of this paper.

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Supplementary materials

Suppl. material 1: The gymnosperm-feeding leafminers and their host plants in North America

Authors: Taibin Chen, Xiaohua Dai, Charles Eiseman

Data type: Number of species

Download file (33.35 kb)

Suppl. material 2: The gymnosperm-feeding leafminers and their host plants in Europe

Authors: Taibin Chen, Xiaohua Dai, Charles Eiseman

Data type: Number of species

Download file (19.06 kb)

Suppl. material 3: Insect families of leafminers on ferns, gymnosperms, angiosperms in North America and Europe

Authors: Taibin Chen, Xiaohua Dai, Charles Eiseman

Data type: Insect families

Download file (18.34 kb)

Endnotes