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Systematic paleontology
Frondicuniculum ichnogen. nov.
Etymology. Classical Latin: frons -dis, a leaf, leafy twig or foliage; and cuniculum-i, meaning a mine, underground passage, hole or pit.
Type ichnospecies. Frondicuniculum lineacurvum ichnosp. nov.
Diagnosis. Elongate-ellipsoidal blotch mines occurring on broadleaved, parallel veined conifer leaves. Long axes of the mines are parallel to leaf venation. Frass, when present, is densely packed, composed of spheroidal pellets surrounded by amorphous matter, often positioned along one margin of the mine. Leaf veins within mines are distorted.
Frondicuniculum lineacurvum ichnosp. nov.
Etymology. Classical Latin: linea-e, a string, linen thread, or drawn line; and curvus–a –um, bent, bowed, arched, or curved.
Holotype. MPEF-Pb 6336 (Fig. 1d–f and Supplementary Fig. 3a–e), Laguna del Hunco quarry LH610, early Eocene, Chubut Province, Argentina.
Paratypes. MPEF-Pb 3160 (Laguna del Hunco quarry LH6, Supplementary Fig. 3f), USNM 545226 (Río Pichileufú historical collection48, Fig. 1g, h and Supplementary Fig. 4a, b).
Diagnosis. As for the genus, with smooth, linear to gently curving mine margins.
Description. An elongate-ellipsoidal blotch mine positioned along leaf margin, long axis parallel to leaf veins, mine margins well defined, linear to gently curving. Mine dimensions 7.2–50.0 mm long by 2.0–10.0 mm wide. Frass, when present, composed of spherical or hemispherical pellets measuring 0.04–0.12 mm in diameter and surrounded by dark, amorphous matter. Frass pellets mostly positioned near mine margin and may be replaced by surrounding amber with original frass material not preserved. Reaction rim 0.1–0.3 mm wide present at contact between mine margins and surrounding leaf tissue. Individual specimen descriptions of holotype and paratypes provided in Supplementary Note 1.
Occurrence. Huitrera Formation, Laguna del Hunco (early Eocene, Chubut Province, Argentina) and Río Pichileufú (middle Eocene, Río Negro Province, Argentina), on host plant Agathis zamunerae Wilf.
Repositories. Museo Paleontológico Egidio Feruglio, Trelew, Chubut, Argentina (MPEF-Pb), and Smithsonian Institution, National Museum of Natural History (USNM).
Frondicuniculum flexuosum ichnosp. nov.
Etymology. Classical Latin: flexuosus –a –um, full of winding turns, bent, or crooked.
Holotype. MPEF-Pb 5970 (Fig. 1a–c and Supplementary Fig. 2a–c), Palacio de los Loros 2 (PL2)42, Salamanca Formation, early Paleocene, Chubut Province, Argentina.
Paratypes. MPEF-Pb 5960 (Supplementary Fig. 2d, e), MPEF-Pb 6007 (Supplementary Fig. 2f, g), MPEF-Pb 6001 (Supplementary Fig. 2h–j), all from the PL2 locality.
Diagnosis. As for the genus, with wavy mine margins.
Description. An elongate-ellipsoidal blotch mine with gentle to strongly undulatory margins having a raised, wrinkly appearance. Mine positioned along leaf margin, long axis of the mine parallel to leaf veins. Mine dimensions 11.4–35.2 mm long by 1.2–9.4 mm wide. Frass, when present, composed of spheroidal pellets measuring ca. 0.1 mm in diameter and surrounded by smaller fragments of amorphous frass. Frass distributed throughout mine or positioned laterally near one margin of the mine. Mine margins 0.2–8.0 mm wide. Individual specimen descriptions of holotype and paratypes provided in Supplementary Note 1.
Occurrence. Palacio de los Loros 2 locality; Salamanca Formation, early Paleocene; Chubut Province, Argentina, on host plant Agathis immortalis Escapa, Iglesias, Wilf, Catalano, Caraballo et Cúneo.
Repository. Museo Paleontológico Egidio Feruglio, Trelew, Chubut, Argentina (MPEF-Pb).
Remarks
For clarity, we note that the new zoological typifications and identifications assigned here refer only to the insect-damaged areas (i.e., trace fossils) of the cited fossil material, which often has separate botanical typification and identification under the same repository numbers as defined by Wilf et al.22 for Agathis zamunerae and Escapa et al.7 for Agathis immortalis. Morphologically similar, elongate-ellipsoidal blotch mines are associated with Agathis at PL2 (early Paleocene, 4 specimens), LH (early Eocene, 2 specimens), and RP (early/middle Eocene, 1 specimen), as well as Cretaceous cf. Agathis (see next paragraph), with minor differences in their margin structure. Frondicuniculum flexuosum mines have undulatory, wrinkled margins (Fig. 1a, c, and Supplementary Fig. 2a–j), whereas F. lineacurvum mines (Fig. 1d–h and Supplementary Figs. 3a–f, 4a, b) have smooth, gently curving margins. However, the overall shape, position on leaves, frass characters, and persistence through ca. 18 myr on the same host genus from the same region suggest that the mines were made by similar, probably closely related leaf-mining insects.
A blotch mine positioned along the central axis of a cf. Agathis leaf from the Maastrichtian Lefipán Formation is characterized by an elongate-ellipsoidal shape with its long axis parallel to the leaf veins and smooth, gently curved margins (Fig. 1i and Supplementary Fig. 1a–c). The mine lacks frass, which may be a preservational effect, and otherwise could be the same as Frondicuniculum lineacurvum. Because of the preservation and because there is only one specimen, or possibly two (Supplementary Fig. 1d), we did not assign a formal name to this specimen. However, the overall similarity of Cretaceous and Paleocene blotch mines on Agathis (elongate-elliposidal shape, smooth margins, distorted leaf veins) is noteworthy as the first likely evidence of a Cretaceous-Paleogene (K-Pg) boundary crossing leaf-mine association on closely related plants. Until now, no evidence has been found of surviving K-Pg leaf-mine associations within regional Maastrichtian and Danian floras anywhere in the world46,49,50.
Another probable blotch-mine type from LH and RP (Eocene) has a linear trajectory and is oriented parallel to the leaf veins, exhibiting breached epidermal tissue (DT251; Fig. 2a, b and see Supplementary Note 1 for detailed descriptions). The putative mines have a similar appearance to slot feeding characterized by elongate holes, although their smooth, gently curving margins suggest a leaf-mining origin. Some of these mine-like structures are flanked by flaps of epidermal tissue, attributable to breaching of the tissue due to environmental factors such as in vivo abrasion (Fig. 2a). The margins along the field of damage are smooth and sometimes influenced by leaf veins. We found similar damage as possible mines on modern Australian Agathis robusta (Fig. 2c and Supplementary Fig. 5m, Supplementary Note 1), featuring an elongate-ellipsoidal shape oriented parallel to the leaf veins. Like the fossils, the epidermal tissue of the extant mines is often breached (Fig. 2c and Supplementary Fig. 5m), leaving flaps of unconsumed tissue surrounded by a thin, darkened rim of reaction tissue.
Fig. 2: External foliage feeding, blotch and serpentine mining, galling, and possible armored scale insect remains (Diaspididae) on fossil and extant Agathis.

a Putative blotch mine, or slot feeding, characterized by parallel sides and flaps of necrotic tissue on A. zamunerae (early Eocene, LH13, MPEF-Pb 6361). b Elongate blotch mine with breached epidermal tissue and thickened reaction rim on A. zamunerae (early middle Eocene, RP, USNM 545227). c Blotch mine, or possible slot feeding, flanked by flap of epidermal tissue on A. robusta (Queensland, Australia, (A.K. Irvine 00417 (A)). d Linear serpentine mines following leaf venation on cf. Agathis (latest Cretaceous, DT139; MPEF-Pb 9836). e Detail of frass trail in d. f Semicircular excision into the leaf margin on A. immortalis (Danian, PL2, MPEF-Pb 6091). g Shallow excision into the leaf margin with vein stringers on A. zamunerae (early Eocene, LH13, MPEF-Pb 6361). h Two adjacent excisions into the leaf margin on A. zamunerae (early/middle Eocene, RP, BAR 5002). i Two adjacent excisions into the leaf margin of A. moorei (New Caledonia, E 00106192). j Ellipsoidal gall with thickened walls surrounding unthickened epidermal tissue on A. immortalis (Danian, PL2, MPEF-Pb 9767). k Ellipsoidal gall with circular exit hole on A. ovata (New Caledonia, E 00399687). l Possible armored scale cover (Diaspididae) with concentric growth rings on A. immortalis (Danian, PL2, MPEF-Pb 5996). m Possible diaspidid scale cover on A. zamunerae, under epifluorescence (early Eocene, LH27, MPEF-Pb 6383). n Possible diaspidid scale covers on A. zamunerae, under epifluorescence (early/middle Eocene, RP, USNM 545228). o Possible diaspidid scale cover with concentric growth rings indicating two larval and an adult growth stage on A. zamunerae, under epifluorescence (middle Eocene, RP, USNM 545228). p Diaspidid scale insects that induced pit galls on A. macrophylla (Fiji, GH 01153259). q Rust fungus (Pucciniales) with aecia on a circular spot on A. zamunerae (early Eocene, LH06, MPEF-Pb 6303). r Kauri rust (Aecidium fragiforme) on A. macrophylla (Vanuatu, S.F. Kajewski 282 (K)).

Full size image

Only two extant leaf-mining insects have been documented in association with Agathis (Supplementary Data 1), both on A. australis of New Zealand, although their mines are not similar to the fossils. Larvae of the leaf blotch-miner moth Parectopa leucocyma (Lepidoptera: Gracillariidae) initially form small blotch mines that transition to linear epidermal mines and then galls39. Microlamia pygmaea, a longhorn beetle (Coleoptera: Cerambycidae), mines dead leaves on fallen branches51. In our survey of extant Agathis, we found numerous examples of blotch mines similar to our fossils on six host species that span much of the modern range of the genus (Fig. 1j–m, Supplementary Fig. 5a–f, Supplementary Note 1). The extant blotch mines, previously undocumented to our knowledge, are typically elongate-ellipsoidal and exhibit many similarities to the fossils, suggesting geologically long-term behaviors with origins in the late Mesozoic and early Cenozoic. Most mine trajectories occur along the leaf margins (Fig. 1j–m), although some course along the central axes of leaves (Supplementary Fig. 5c). The long axes of the extant blotch mines are parallel to leaf venation (Fig. 1j–m) as in the fossils. Margins of the mines are smooth to wavy.
In order to assess potential convergence of leaf mine morphologies associated with related conifers that have similar leaf architecture to Agathis, we also compared extant mines on Araucaria (Araucariaceae) and members of the Podocarpaceae family, including Nageia, Afrocarpus, Sundacarpus, and Podocarpus. Araucarivora gentilii Hodges (Elachistidae) caterpillars mine leaves of Araucaria araucana in Argentina and Chile52. Mines begin with a short serpentine phase and then expand into a raised, circular to polylobate blotch mine. A circular exit hole is typically positioned near the margin of the blotch mine. The fossil Agathis blotch mines (Fig. 1a–i and Supplementary Figs. 1–4) differ in that they are elongate and lack a serpentine phase. We did not find any other blotch mine morphologies on Araucaria herbarium specimens throughout the range of the genus (parts of South America and Australasia). Three leaf-mining taxa have been described on Podocarpus. Phyllocnistis podocarpa (Lepidoptera: Gracillariidae) larvae mine Podocarpus macrophyllus leaves in Japan, creating serpentine mines with overlapping paths that often form into a blotch, although their zigzag frass trail is distinct from the fossil Agathis blotch mines53. In New Zealand, Podocarpus totara hosts two leaf miners, including Chrysorthenches polita (Lepidoptera: Glyphipterigidae), whose mines have not been described54, and Peristoreus flavitarsis (Coleoptera: Curculionidae)55. The mines of Peristoreus flavitarsis are a possible extant analog to the fossil Agathis mines, in addition to similar mines we found on extant Agathis (Fig. 1j–m and Supplementary Fig. 5). The mines are full depth and typically span the width of the leaf. Frass pellets are often deposited along portions of the mine margin at the edge of the leaf. Individual larvae make mines on multiple leaves. Before pupating in the soil or litter, the larva chews a circular hole through the epidermis on the abaxial side of the leaf55. We found other putative blotch mines on herbarium sheets of Podocarpus with similar morphologies to those on extant and fossil Agathis, including on Podocarpus ingensis from Bolivia, Podocarpus oleifolius from Colombia, and Podocarpus urbanii from Jamaica. We did not find any comparable mines on herbarium specimens of Afrocarpus, Nageia, or Sundacarpus.
Leaf mines have been recognized on other broadleaved, parallel-veined gymnosperms from the Mesozoic, although Frondicuniculum is distinguished from all the Mesozoic examples by its blotch morphology and lack of a serpentine phase. Similar to our Cretaceous specimens (Fig. 2d, e, and Supplementary Fig. 1e, f), unnamed mines on the voltzialean conifer Heidiphyllum elongatum, from the Late Triassic (Carnian) of the Karoo Basin in South Africa56,57, exhibit an elongate, parallel-sided, rectilinear path with spheroidal pellets often deposited in an approximate meniscate pattern. Triassohyponomus dinmorensis mines, also on H. elongatum but from the Blackstone Formation (Middle Triassic) in Australia58, are serpentine and have an extensive, tightly sinusoidal to meniscate pattern. Fossafolia offae on Liaoningocladus boii from the Early Cretaceous Yixian Formation of northeast China begins as a serpentine mine with an intestiniform frass trail and transitions to a blotch phase59. The blotch mines on Patagonian fossil and living Old World Agathis therefore appear to represent part of a suite of leaf mining insects of uncertain interrelationships that has colonized parallel-veined, broadleaved seed plants since the Mesozoic, but which nevertheless are distinct from the Mesozoic examples in producing the blotch-mine morphology with no serpentine phase.
Additional damage diversity
In addition to leaf mines, fossil and extant Agathis are associated with a variety of other insect feeding types (Table 1), which we sketch here while details are being prepared separately. External foliage feeding includes small circular holes (DT1, DT2; Table 1), semicircular excisions into leaf margins (DT12; Fig. 2f–h), and swaths of surface feeding (DT29). A similar spectrum of damage is found on extant Agathis throughout its range (Fig. 2i). However, many types of external foliage-feeding damage can be made by a variety of insects with mandibulate mouthparts across several taxonomic orders60, and their presence at multiple fossil and modern sites does not necessarily indicate that the same suite of closely-related insect groups produced the damage.
Table 1 Insect damage types on fossil and extant Agathis.
Full size table

Four gall DTs are associated with fossil Agathis in Patagonia, including nondiagnostic, dark circular galls (DT32; Lef and LH), circular galls with a nonhardened center surrounded by a thickened outer rim (DT11; PL2), and columnar galls (DT116; PL2). Moreover, at PL2, A. immortalis is associated with ellipsoidal galls bearing a thickened outer wall surrounding epidermal tissue with files of cells. The center of each gall is marked by a circular dot representing the central chamber or exit hole (Fig. 2j). The fossils resemble undescribed ellipsoidal galls on A. ovata from New Caledonia, which are characterized by a raised rim of thickened tissue surrounding a flat, epidermal surface with a circular exit hole (Fig. 2k). The only previously documented galling insect on extant Agathis is Conifericoccus agathidis (Hemiptera: Margarodidae), the kauri coccid, whose second-instar nymphs induce blister galls that have caused extensive defoliation of Agathis robusta in Australia61. Nevertheless, we found abundant and diverse gall morphologies on extant Agathis (Fig. 2k and Table 1).
Possible covers of female armored scale insects (Diaspididae) occur on Agathis at PL2 (Fig. 2l), LH (Fig. 2m), and RP (Fig. 2n, o). At PL2, the covers are found on leaves and a cone scale7. The dorsal covers are characterized by concentric growth rings made during the construction of the cover through two instars and an adult phase (Fig. 2l–o). Ventral covers surround the dorsal covers (Fig. 2m) and, in some cases, appear to be deeply set in the leaf tissue and leave a columnar or circular pit when detached. We caution that other interpretations of these structures remain possible because some of their features are not present on extant diaspidid covers (off-center indent or hole on dorsal covers) or are atypical (ventral cover structure surrounding dorsal cover; only adult female covers are present). The possible scale covers, including the-off center indent, are very similar to structures assigned to Diaspididae from the Late Cretaceous of New Zealand and Australia62, and comparable scale covers are associated with angiosperm leaves from the Eocene of Germany63 and Miocene of New Zealand64. On extant Agathis, diaspidid scales previously have been documented on three species in New Zealand and Australia (Supplementary Data 1). We found diaspidids on Agathis herbarium specimens from New Caledonia and Fiji, including an unidentified diaspidid species that induced pit galls on A. macrophylla from Fiji (Fig. 2p).
A probable rust fungus (Pucciniales), characterized by rings of circular to oval aecia on a circular gall, is associated with Agathis zamunerae at LH (Fig. 2q). Two species of rust fungi in the genus Aecidium parasitize extant Agathis: Aecidium fragiforme from Oceania and Malesia and Aecidium balansae in New Caledonia (Fig. 2r)40,65. Aecidium on extant Agathis produces galls covered in yellow aecia (Fig. 2p). The very similar morphologies of the fossil and extant rust on Agathis suggest long-term, persistent associations reaching back to at least the early Eocene. More

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