Culcita Remberi Sp. Nov., an Understory Fern of Cyatheales from the Miocene of Northern Idaho

Home , Calochlaena, Cibotium, Coniopteris, Culcita macrocarpa, Cyatheales, Tree fern

CULCITA REMBERI SP. NOV., AN UNDERSTORY FERN OF CYATHEALES FROM THE MIOCENE OF NORTHERN IDAHO

Jerald B. Pinson,1,* Steven R. Manchester,† and Emily B. Sessa*

*Department of Biology, University of Florida, Box 118525, Gainesville, Florida 32611, USA; and †Florida Museum of Natural History, University of Florida, Box 118525, Gainesville, Florida 32611, USA

Editor: Michael T. Dunn

Premise of research. Excavations at the Clarkia fossil beds in northern Idaho have recovered numerous exceptionally well-preserved plant fossils over the past 45 years. We report on a compression fossil of a fertile frond from a tree fern found at the Emerald Creek locality. Methodology. Intact leaf material was liberated from the substrate by wetting with hydroﬂuoric acid followed by submersion in a water bath. The lamina was preserved between sheets of acetate and photographed, and fertile pinnules with sporangia were mounted on aluminum stubs and imaged with scanning electron microscopy. Spores were released from sporangia after incubation in Schulz’s solution and treatment with KOH. Pivotal results. The specimen is similar to members of several extant fern lineages, including Hymenophyl- laceae, Dennstaedtiaceae, and the tree fern order Cyatheales. It shares with these groups the possession of oblong, marginal sori, although the sori of the specimen are most similar to the cup-shaped sori of Dennstaedtiaceae and the bivalvate sori of Culcitaceae. The fossil also has sporangia, each with a complete, uninterrupted, oblique annulus, which is strongly associated with Culcitaceae. Conclusions. On the basis of its overall lamina morphology and details of the sori and especially the sporangia, we conclude that this specimen belongs to an extinct species of the monogeneric tree fern family Culcitaceae. The occurrence of a tree fern in the temperate plant community of the Miocene Clarkia locality is unexpected but not incompatible with the habitat preferences of this genus, as the two extant species of Culcita are found in montane altitudes and temperate forests elsewhere in the world.

Keywords: fossil, Miocene, Polypodiopsida, sporangia, tree fern.

Introduction suggests that temperatures in Idaho were warmer during the mid- Miocene than they are today (Smiley and Rember 1981). The Clarkia fossil beds in northern Idaho have been the source This study reports on the discovery of a compression fossil of of exceptionally well-preserved impression and compression fos- a fertile frond from a tree fern found at the Emerald Creek local- sils since their discovery in 1972 (Smiley and Rember 1981). De- ity near Clarkia, Idaho. While ferns are nowhere near as ubiq- position occurred during the middle Miocene, when a volcanic uitous as spermatophytes at the site, fossilized remains of Equi- eruption dammed the adjacent St. Maries River at approximately setum, Osmunda, and Polypodium have been reported (Smiley 16–15.4 Ma (Ladderud et al. 2015). Many of the leaf fossils re- et al. 1975). Still, the recovery of only one fossilized tree fern tain their original pigmentation until exposed to air, after which fragment, compared to the thousands of conifer and angio- they rapidly oxidize, and their pristine condition has even al- sperm specimens at Clarkia (Smiley and Rember 1981), under- lowed for isolation of flavonoids (Giannasi and Niklas 1977) scores the rarity of the specimen. Here we present a description and DNA in a few instances (Golenberg 1991; Soltis et al. 1992; of the morphology of the leaf, sporangia, and spores, paying Kim et al. 2004). Studies reconstructing the plant communities particular attention to characters that distinguish it from species present at the time of deposition lead to the conclusion that the with similar morphology and allow us to hypothesize its closest local flora was a temperate deciduous forest consisting mainly living relatives. of conifers (Kvaček and Rember 2000) and angiosperms (Smiley and Rember 1985), taxonomically similar to forest communities Material and Methods present today in both eastern Asia and the southeastern United States (Smiley et al. 1975; Smiley and Rember 1981, 1985). This Material was obtained from the Emerald Creek locality known as University of Idaho P-37 (UF locality 18630, 47701.9720N 1 Author for correspondence; email: jbp4166@ufl.edu. 116720.3070W) in an excavation adjacent to the Rember resi- Manuscript received January 2018; revised manuscript received May 2018; dence, Benewah County, Idaho. The intact compression fossil electronically published August 3, 2018. was lifted from the sediment by wetting the surface of the lam-

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This content downloaded from 128.227.126.194 on November 05, 2018 07:56:04 AM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). 636 INTERNATIONAL JOURNAL OF PLANT SCIENCES ina with concentrated hydrofluoric acid for a few minutes, then clude members with similar marginal, oblong sori, taxa in the immersing the specimen in a water bath and manipulating the Hymenophyllaceae have extremely thin laminar tissue that is loosened lamina onto a piece of plastic window screening, only one or a few cell layers thick and indusia that are generally which was carefully removed by hand from the water bath and more circular than elongated (Tryon and Tryon 1982), neither inverted onto a piece of acetate previously trimmed to an appro- of which applies to the fossil. Of the two remaining groups, priate size. Drops of glycerine were then added and another sheet Dennstaedtiaceae and the tree ferns, the fossil’s sori are most of acetate applied to archive the lamina as a glycerine fossil sand- similar to both Dennstaedtiaceae and Culcitaceae. Members wich on acetate. Portions of pinnules with sori were detached of Dennstaedtiaceae have cup-shaped sori that are similar in ap- and mounted on aluminum stubs for scanning electron micros- pearance to the bivalvate sori of Culcitaceae (Tryon and Tryon copy (SEM). These were coated with palladium with a Denton 1982). However, because of the oxidation of the sori in the fos- DeskV sputter-coater and imaged with a Hitachi SU5000 Schottky sil specimen, we were unable to determine which of these two Field-Emission SEM. Transmitted-light microscopy of sporan- the fossil possesses. gia and spores was performed with a Nikon Eclipse microscope. Sporangia in Dennstaedtiaceae have a vertical to slightly oblique To free the spores from the surrounding indusia and sporan- annulus interrupted at the stalk (Tryon and Tryon 1982). The gia, maceration of tissue was first attempted with KOH, to no fossil, however, displays sporangia with a complete, uninterrupted, effect. We then incubated the tissue with Schultz’s solution for oblique annulus (fig. 2), characters strongly associated with the 5 min, which, when washed in water and followed by brief treat- family Culcitaceae (Sen 1968; Tryon and Tryon 1982). The ment with 5% KOH, cleared the sporangia and released the unique leaf morphology of the fossil fragment separates it from spores. other potentially closely related (and otherwise morphologically similar) genera of tree ferns; for example, the lamina is at least Results bipinnate and is highly dissected, the latter feature distinguishing it from genera such as Cibotium. On the basis of these characters Taxonomic Treatment considered jointly, we conclude that the fossil is an extinct mem- ber of the monogeneric tree fern family Culcitaceae. Other char- Class—Polypodiopsida acters, such as the grooved rachis and unornamented trilete spores, while not unique to Culcitaceae, further support the consignment Order—Cyatheales of the fossil to this family.

Family—Culcitaceae Discussion fl Species—Culcita remberi Pinson, Manchester & Sessa This extinct species belonged to a ora that included many sp. nov. (Figs. 1, 2D, 2F) temperate elements, for example, Metasequoia, Cunninghamia, Calocedrus, Taxus, Platanus, Liquidambar, Cercidiphyllum, Holotype. UF 18630-61360, designated here, deposited in Betula, Ostrya, Paliurus, Prunus, Pterocarya, and Fagus (based the Paleobotanical Collection of the Florida Museum of Nat- on examination of specimens in the University of Florida Paleo- ural History, University of Florida. botanical Collection at the Florida Museum of Natural History). Diagnosis. The fossil is a fragment of a fertile leaf approx- The presence of a tree fern in a such an environment might ini- imately 3 cm in width and 7 cm in length. The fragment is at tially seem suspicious. The two extant Culcita species, however, least twice pinnate and the margins entire. Pinnules are deltoid do not grow exclusively, or even primarily, in warm tropical en- and taper slightly toward the apex of the fragment. The adaxial vironments, nor do they have the prominent vertical trunk asso- surface of the rachis is grooved. Sori are oblong and marginal, ciated with most other extant tree ferns. The fronds are large, attached to a single prominent vein and with an indusium com- reaching up to 3 m in length, but the trunk consists only of a posed partially of laminar tissue. The sori are located exclusively small, prostrate rhizome, relegating these plants to the under- one per pinnule lobe. Sporangia have an oblique, complete an- story (Large and Braggins 2004). These rhizomes have only “ ” nulus composed of approximately 34 cells. Spores are trilete the semblance of trunks because of persistent petiole bases, fi and unornamented and are approximately 30 mm in width. along with hair and root bers (White and Turner 1988), as op- Etymology. We name this species after the discoverer of the posed to the vertical rhizomes of other tree ferns. fossil, William C. Rember, who has worked extensively on the Of the two extant Culcita species, Culcita coniifolia grows in Clarkia Beds since their initial discovery. the New World and Culcita macrocarpa in the Old. The former can be found in the montane and submontane rainforests of Comparisons to Extant Ferns Central and South America, including Jamaica, Cuba, and the island of Hispaniola, from 1500 to 3500 m in elevation (Large Because of the fragmentary nature of the fossil (fig. 1) and the and Braggins 2004). The montane climates of the Neotropics homoplasious nature of some of its key characters in extant have substantially lower temperatures than the surrounding low- ferns, its affinity to an extant fern lineage is not immediately rec- lands, with a mean average temperature of 127–207C in the lower ognizable without close scrutiny. The general morphology and montane rainforests (1000–2500 m) and between 127 and 177C marginal, oblong sori observable on the fossil (figs. 1, 2) allow in the upper montane regions (2500–3500 m; Webster 1995). us to narrow its potential lineage to several families, including Culcita macrocarpa grows throughout the Iberian Peninsula as Hymenophyllaceae and Dennstaedtiaceae, as well as a few fam- well as along the northwest coast of Africa and in the Canary ilies in the tree fern order Cyatheales. While these groups all in- Islands and the Azores, where it can be found at low elevations,

Fig. 1 Fossil foliage of Culcita remberi sp. nov. Holotype: UF 18630-61360. A, Fertile frond; bar p 1 cm. B, Detail of pinnules; bar p 2 mm. C, Detail of sorus, transmitted and reflected light; bar p 0.5 mm. D, Detail of sorus and contained sporangia by reflected light; bar p 0.5 mm. E, Same sorus shown in D, by SEM, with portion of indusium removed to reveal sporangia; bar p 0.5 mm. F, Another sorus; bar p 0.5 mm. G, An- nulate sporangia; bar p 150 mm. H, Sporangium with wall ruptured to show spores; bar p 75 mm. I, Detail of spores within sporangium; bar p 40 mm. J, Details of spores, highlighting trilete scars and unornamented surface; bar p 30 mm. typically around 350 m. In Spain and Portugal, it often grows in per individual. Nevertheless, the available characters allow for a warm, temperate oak forests (Large and Braggins 2004). Neither secure identification of Culcita, indicating that this genus was for- the temperature nor the physiography of the Clarkia Beds during merly distributed outside of its modern-day range. the Miocene are therefore out of character for the genus, al- To our knowledge, this is the first published account of a though the presence of just a single fossil specimen to date likely Culcita fossil specimen verified with details of sporangia as well indicates a low abundance of the species at the site. We can also as leaf morphology, although Holttum (1964) suggested that a expect a taxonomic bias, whereby deciduous-leaved angiosperms fossilized stem from the Eocene of Bournemouth, England, may will be overrepresented in lake deposits, compared to perennial belong to the genus. The specimen detailed in our study closely ferns and other herbaceous plants that shed relatively few leaves resembles an older fossil species, Coniopteris blomstrandii (Heer)

This content downloaded from 128.227.126.194 on November 05, 2018 07:56:04 AM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). Fig. 2 Morphological comparison of extant and fossil species. A, Fertile frond of Culcita coniifolia, abaxial surface (courtesy of Robbin Moran). B, Fertile frond of Culcita macrocarpa, abaxial surface (courtesy of Juan Manuel Pérez de Ana). C, Trilete spores of C. coniifolia; bar p 10 mm (courtesy of Robbin Moran; specimen voucher: Burger and Liesner 6497 [NY]). D, Fossil sporangia of Culcita remberi, sp. nov. by transmitted-light microscopy, highlighting the oblique curvature of the annulus in relation to the stalk as well as the complete ring of annular cells; bar p 0.5 mm. E, Frond of C. coniifolia, adaxial surface, highlighting the grooved rachis and costae (courtesy of Robbin Moran). F, Frond of C. remberi, adaxial surface, highlighting a groove (arrows) along the main rachis; bar p 2 mm.

Kvaček and Manum 1993, from the Paleogene of Spitsbergen, ilies. To our knowledge, there are no known fossils in the Pla- both in macromorphology of the frond and morphology of the giogyraceae, the sister family to Culcitaceae. The fossil record spores in situ. Kvaček and Manum applied the fossil-genus name of the next most closely related family (Loxsomataceae) consists Coniopteris to their specimen because of difficulties distinguish- of a fossilized rhizome assigned to Loxsomopteris from the ing between species belonging to Dennstaedtiaceae and the tree Lower Cretaceous of Maryland (Skog 1976) and several pre- fern family Dicksoniaceae. They considered their material to rep- served rhizome specimens across six or seven species assigned resent Dicksoniaceae rather than Dennstaedtiaceae, apparently to the morphogenus Solenostelopteris, which may or may not on the basis of spore morphology, but could not place it in a par- all belong to the Loxsomataceae (Little et al. 2006). The paucity ticular modern genus and so used Coniopteris, which had previ- of fossils in Culcitaceae and related families therefore makes the ously been applied only to Mesozoic ferns. They were unable to specimen described here a rare and unique addition to the fossil observe sporangial morphology in their fossils. The fossil-genus record of the tree fern alliance. name Coniopteris, as amended by Kvaček and Manum, remains useful to accommodate specimens of similar morphology for which placement in a modern genus cannot be made securely Acknowledgments because of limits of preservation. In our case, the exquisite details of preservation give us confidence in our assignment of this We are grateful to Dr. William C. Rember, who collected and specimen to Culcita. prepared the specimen and kindly donated it to the Florida Mu- The order Cyatheales has a rich fossil record dating back to seum of Natural History for this investigation. We are also grate- the Triassic (252.17–201.3 Ma), with a global distribution (Tay- ful to Dr. Robbin Moran, who provided helpful feedback on lor et al. 2009). However, while there are several hundred fossil possible affinities of the fossil specimen. We also thank two anon- specimens from families such as Dicksoniaceae and Cyathea- ymous reviewers who provided helpful comments on the man- ceae, in the latter of which stems are often well preserved, fossils uscript. This investigation was supported in part by National are sparse to nonexistent in Culcitaceae and closely related fam- Science Foundation grant EAR 1338285 to S. R. Manchester.

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