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A left-handed fern twiner in a Permian swamp forest
Current Biology
Magazine Correspondence
A left-handed fern twiner in a Permian swamp forest Weiming Zhou1, Dandan Li1,2, Josef Pšenicˇka1,3, C. Kevin Boyce4, and Jun Wang1,2,* The twining habit is a climbing strategy that helps slender plants grow upward by using circumnutation around other plants. In geological history, climbing may have already been present in the first Middle Devonian forests, as indicated by possible climbers among aneurophytalean progymnosperms [1] and lycopsids [2]. By the late
Carboniferous, climbing was both more common and diverse — preserved in swamp forests with modes of attachment ranging from aerial roots to appendages modified into hooks and tendrils on the leaves [3]. However, all of these diagnoses of a climbing habit are based upon either indirect morphological characteristics of the purported climber or on direct physical contact with a host plant, but without direct preservation of twining [3,4]. Permineralized epiphytes have been preserved in the Carboniferous [5], but the interpretation of scars purported to have been caused by twiners that have been found on trunk compressions of potential host-plants has been questioned [5] (see Supplemental Information). Direct preservation of a climber engaged in true twining around
B
A
D
a host has only been documented in the Miocene Shanwang Formation of Eastern China, albeit with the identity of the twiner difficult to establish and likely to be a self-twiner [6]. Here, we report a climbing fern engaged in lefthanded twining around a seed plant from the early Permian Wuda Tuff fossil Lagerstätte of Inner Mongolia, China [7]. Moreover, the host plant is likely to also be a climber based on its overall form. Such a climber-climbing-a-climber phenomenon signals the potential ecological complexity of late Paleozoic forests. For the first time prior to the Neogene, twining is directly preserved with a smooth axis 1.2 mm in diameter encircling a larger 4 mm axis (Figure 1A) with prickles (Figure S1A) and two secondary branches. In position P1, H
Axis B Axes C Axis D P3
Axis A
E
C
P2
F
G
P1
Figure 1. Twining specimens collected from the early Permian swamp forest of the Wuda Coalfield. (A) Compression fossil of a slender axis A wound around a wider axis B. Specimen PB23100, scale is 1 cm. (B–C) Enlargements of (A) showing the contacts between the axes A and B, scales are 2 mm. (D) Cross-section of axis B made from the red dotted line in Figure 1A, scale is 1 mm. (E) Crosssection of axes A (green arrowhead) and B made from the green dotted line in Figure 1A. A secondary axis extends from the left side of axis B (red arrowhead), scale is 500 µm. (F) Enlargement of axis A showing a slightly C-shaped xylem strand without any secondary tissues, scale is 100 µm. (G) Diagram of (F), scale is 100 µm. (H) Another twining specimen showing at least four axes C winding around another relatively wider axis D, scale is 2 cm.
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Current Biology 29, R1163–R1173, November 18, 2019 © 2019 Elsevier Ltd.
Current Biology
Magazine axis A is overlain by axis B (Figure 1C). In position P2, axis A can be seen to be underlain by axis B, despite being partly damaged during the field excavation (Figure 1C). In position P3, axis A is overlain again by axis B (Figure 1B,E). This complete rotation of axis A around axis B confirms a left-handed twiner. Coalified anatomy is preserved in both axes of this compression fossil. The host, axis B, possesses a eustelic stem anatomy that generally indicates it is a seed plant (Figure 1D). Material with the same stem anatomy and prickle structures is well represented across the fossil collections from the Wuda Tuff (Figure S1I,J,L). Axis B can be classified as Callistophytales on account of clearer anatomy showing pith surrounded by primary xylem bundles and leaf traces, and secondary xylem composed of alternating files of tracheids (1–4 cells wide) and rays (Figure S1L). The twiner, axis A, possesses a slightly C-shaped xylem strand anatomy without any secondary tissues and is thereby interpreted as a fern rachis (Figure 1F,G). The associated plant fragments on the same bedding plane — including a scale-bearing crozier (Figure S1B), hooks (Figure S1C), and a pinna (Figure S1D) — suggest a more specific identity. At this locality, similar hooked structures are known only from two species of Sphenophyllum (Figure S1O,P) and an anachoropterid fern (Figure S1Q–T). The morphologies of the crozier and dentate pinnules are identical to those of the anachoropterid fern (Figure S1Q,T). The proximity to axis A of these fragments suggests that axis A too may belong to an anachoropterid fern. It bears specialized hooked tendrils situated below each penultimate rachis that grow precociously before the expansion of the vegetative pinnules (Figure S1Q). If this identification is correct, the anachoropterid fern may climb by both hooked tendrils and twining rachides. In a second specimen photographed in the field, at least four smooth axes of 1 mm width wind in left-handed helices around a larger axis 8 mm in diameter (labeled C and D, respectively in Figure 1H). The broad axis can be identified as the same callistophytalean plant by the prickles on the stem surface (Figure S1E). One of the narrow twining axes has a secondary axis bearing a pinna (Figure S1H) similar in morphology
to the attached pinna in Figure S1D. The narrow axes are, thus, interpreted to be the same as twining axis A, and suggest a consistent left-handed twining direction for this taxon (Figure S1F,G). The handedness in modern twining taxa is either fixed or occasionally variable. However, more than 90% of modern twiners, including the fern Lygodium, are dominated by righthanded helices [8,9]. It is uncertain why this dextral bias exists in modern twiners. Here, however, discovery of the oldest known twiner indicates a persistent left-handed preference. In the literature, the Callistophytales has been described as scrambling or climbing understory plants [10]. The hosts described here have long and thin stems, less than 1 cm in diameter. The prickles on the stem surface in living climbers, such as those of Rosaceae, can produce frictional resistance in catching or hanging onto other suitable plants. Other specimens of the host plant possess heterophyllous pinnules on their fronds (Figure S1K) with some pinnules modified into pinnate linear lobes that terminate in swollen structures previously interpreted from similar material as adhesive pads (Figure S1M,N) [3]. Therefore, the evidence strongly suggests that the host plant is a climber. The dual-climbing phenomenon is known from modern tropical and subtropical forests (Figure S1U,V), but has never been documented in the fossil record. Although indirect morphological evidence has led to the expectation that the climbing habit was already common in late Carboniferous tropical forest ecosystems, it is nonetheless striking to see here direct preservation of the twining habit together with evidence of the dual-climbing phenomenon (Figure S2), indicating a high degree of ecological complexity in early Permian swamp forests. SUPPLEMENTAL INFORMATION Supplemental Information includes experimental procedures and two figures and can be found with this article online at https:// doi.org/10.1016/j.cub.2019.10.005. ACKNOWLEDGMENTS We are grateful to several technicians of NIGP, including Mei Shengwu, Mao Yongqiang, Yang Dinghua, Chen Youdong, Gao Yang,
Tang Jingjing and Zhang Xuansi for field and experimental assistance. This work is supported by the Strategic Priority Research Program (B) of CAS (XDB18000000, XDB26000000), the National Natural Science Foundation of China (41802011, 41872013, 41530101), the State Key Laboratory of Palaeobiology and Stratigraphy (NIGP) (20182114), the Visiting Professorship for Senior International Scientists of CAS (2016vea004) and the Grant Agency of Czech Republic (19-06728S). AUTHOR CONTRIBUTIONS W.Z. and J.W. designed the research. W.Z. and D.L. collected the specimens. W.Z. and C.K.B. prepared the manuscript. J.P. contributed the callistophytalean study. REFERENCES 1. Stein, W.E., Berry, C.M., Hernick, L.V., and Mannolini, F. (2012). Surprisingly complex community discovered in the mid-Devonian fossil forest at Gilboa. Nature 483, 78–81. 2. Xu, X.H., Berry, C.M., Wang, Y., and Marshall, J.E.A. (2011). A new species of Leclercqia Banks, Bonamo et Grierson (Lycopsida) from the middle Devonian of North Xinjiang, China, with a possible climbing habit. Int. J. Plant Sci. 172, 836–846. 3. Krings, M., Kerp, H., Taylor, T.N., and Taylor, T.E. (2003). How Paleozoic vines and lianas got off the ground: on scrambling and climbing Carboniferous–early Permian pteridosperms. Bot. Rev. 69, 204–224. 4. Burnham, R.J., (2009). An overview of the fossil record of climbers: bejucos, sogas, trepadoras, lianas, cipós, and vines. Revista Brasil. Paleontol. 12, 149–160. 5. DiMichele, W.A., and Falcon-Lang, H.J. (2011). Pennsylvanian ‘fossil forests’ in growth position (T0 assemblages): origin, taphonomic bias and palaeoecological insights. J. Geol. Soc. London 168, 585–605. 6. Wang, Q., Shen, S., and Li, Z.Y. (2013). A lefthanded, stem-twining plant from the Miocene Shanwang Formation of Eastern China. Am. J. Plant Sci. 4, 18–22. 7. Wang, J., Pfefferkorn, H.W., Zhang, Y., and Feng, Z. (2012). Permian vegetational Pompeii from Inner Mongolia and its implications for landscape paleoecology and paleobiogeography of Cathaysia. Proc. Natl. Acad. Sci. USA 109, 4927–4932. 8. Darwin, C. (1867). On the movements and habits of climbing plants. J. Linn. Soc. Lond. Bot. 9, 1–118. 9. Edwards, W., Moles, A.T., and Franks, P. (2007). The global trend in plant twining direction. Global Ecol. Biogeogr. 16, 795–800. 10. DiMichele, W.A., Phillips, T.L., and Pfefferkorn, H.W. (2006) Paleoecology of late Paleozoic pteridosperms from tropical Euramerica. J. Torrey Bot. Soc. 133, 83–118. 1 State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology and Center for Excellence in Life and Paleoenvironment, Chinese Academy of Sciences, Nanjing, China. 2University of Chinese Academy of Sciences, Beijing, China. 3Centre of Palaeobiodiversity, West Bohemian Museum in Pilsen, Pilsen, Czech Republic. 4Geological Sciences, Stanford University, Stanford, CA, USA. *E-mail: [email protected]
Current Biology 29, R1163–R1173, November 18, 2019 R1173
Magazine Correspondence
A left-handed fern twiner in a Permian swamp forest Weiming Zhou1, Dandan Li1,2, Josef Pšenicˇka1,3, C. Kevin Boyce4, and Jun Wang1,2,* The twining habit is a climbing strategy that helps slender plants grow upward by using circumnutation around other plants. In geological history, climbing may have already been present in the first Middle Devonian forests, as indicated by possible climbers among aneurophytalean progymnosperms [1] and lycopsids [2]. By the late
Carboniferous, climbing was both more common and diverse — preserved in swamp forests with modes of attachment ranging from aerial roots to appendages modified into hooks and tendrils on the leaves [3]. However, all of these diagnoses of a climbing habit are based upon either indirect morphological characteristics of the purported climber or on direct physical contact with a host plant, but without direct preservation of twining [3,4]. Permineralized epiphytes have been preserved in the Carboniferous [5], but the interpretation of scars purported to have been caused by twiners that have been found on trunk compressions of potential host-plants has been questioned [5] (see Supplemental Information). Direct preservation of a climber engaged in true twining around
B
A
D
a host has only been documented in the Miocene Shanwang Formation of Eastern China, albeit with the identity of the twiner difficult to establish and likely to be a self-twiner [6]. Here, we report a climbing fern engaged in lefthanded twining around a seed plant from the early Permian Wuda Tuff fossil Lagerstätte of Inner Mongolia, China [7]. Moreover, the host plant is likely to also be a climber based on its overall form. Such a climber-climbing-a-climber phenomenon signals the potential ecological complexity of late Paleozoic forests. For the first time prior to the Neogene, twining is directly preserved with a smooth axis 1.2 mm in diameter encircling a larger 4 mm axis (Figure 1A) with prickles (Figure S1A) and two secondary branches. In position P1, H
Axis B Axes C Axis D P3
Axis A
E
C
P2
F
G
P1
Figure 1. Twining specimens collected from the early Permian swamp forest of the Wuda Coalfield. (A) Compression fossil of a slender axis A wound around a wider axis B. Specimen PB23100, scale is 1 cm. (B–C) Enlargements of (A) showing the contacts between the axes A and B, scales are 2 mm. (D) Cross-section of axis B made from the red dotted line in Figure 1A, scale is 1 mm. (E) Crosssection of axes A (green arrowhead) and B made from the green dotted line in Figure 1A. A secondary axis extends from the left side of axis B (red arrowhead), scale is 500 µm. (F) Enlargement of axis A showing a slightly C-shaped xylem strand without any secondary tissues, scale is 100 µm. (G) Diagram of (F), scale is 100 µm. (H) Another twining specimen showing at least four axes C winding around another relatively wider axis D, scale is 2 cm.
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Current Biology 29, R1163–R1173, November 18, 2019 © 2019 Elsevier Ltd.
Current Biology
Magazine axis A is overlain by axis B (Figure 1C). In position P2, axis A can be seen to be underlain by axis B, despite being partly damaged during the field excavation (Figure 1C). In position P3, axis A is overlain again by axis B (Figure 1B,E). This complete rotation of axis A around axis B confirms a left-handed twiner. Coalified anatomy is preserved in both axes of this compression fossil. The host, axis B, possesses a eustelic stem anatomy that generally indicates it is a seed plant (Figure 1D). Material with the same stem anatomy and prickle structures is well represented across the fossil collections from the Wuda Tuff (Figure S1I,J,L). Axis B can be classified as Callistophytales on account of clearer anatomy showing pith surrounded by primary xylem bundles and leaf traces, and secondary xylem composed of alternating files of tracheids (1–4 cells wide) and rays (Figure S1L). The twiner, axis A, possesses a slightly C-shaped xylem strand anatomy without any secondary tissues and is thereby interpreted as a fern rachis (Figure 1F,G). The associated plant fragments on the same bedding plane — including a scale-bearing crozier (Figure S1B), hooks (Figure S1C), and a pinna (Figure S1D) — suggest a more specific identity. At this locality, similar hooked structures are known only from two species of Sphenophyllum (Figure S1O,P) and an anachoropterid fern (Figure S1Q–T). The morphologies of the crozier and dentate pinnules are identical to those of the anachoropterid fern (Figure S1Q,T). The proximity to axis A of these fragments suggests that axis A too may belong to an anachoropterid fern. It bears specialized hooked tendrils situated below each penultimate rachis that grow precociously before the expansion of the vegetative pinnules (Figure S1Q). If this identification is correct, the anachoropterid fern may climb by both hooked tendrils and twining rachides. In a second specimen photographed in the field, at least four smooth axes of 1 mm width wind in left-handed helices around a larger axis 8 mm in diameter (labeled C and D, respectively in Figure 1H). The broad axis can be identified as the same callistophytalean plant by the prickles on the stem surface (Figure S1E). One of the narrow twining axes has a secondary axis bearing a pinna (Figure S1H) similar in morphology
to the attached pinna in Figure S1D. The narrow axes are, thus, interpreted to be the same as twining axis A, and suggest a consistent left-handed twining direction for this taxon (Figure S1F,G). The handedness in modern twining taxa is either fixed or occasionally variable. However, more than 90% of modern twiners, including the fern Lygodium, are dominated by righthanded helices [8,9]. It is uncertain why this dextral bias exists in modern twiners. Here, however, discovery of the oldest known twiner indicates a persistent left-handed preference. In the literature, the Callistophytales has been described as scrambling or climbing understory plants [10]. The hosts described here have long and thin stems, less than 1 cm in diameter. The prickles on the stem surface in living climbers, such as those of Rosaceae, can produce frictional resistance in catching or hanging onto other suitable plants. Other specimens of the host plant possess heterophyllous pinnules on their fronds (Figure S1K) with some pinnules modified into pinnate linear lobes that terminate in swollen structures previously interpreted from similar material as adhesive pads (Figure S1M,N) [3]. Therefore, the evidence strongly suggests that the host plant is a climber. The dual-climbing phenomenon is known from modern tropical and subtropical forests (Figure S1U,V), but has never been documented in the fossil record. Although indirect morphological evidence has led to the expectation that the climbing habit was already common in late Carboniferous tropical forest ecosystems, it is nonetheless striking to see here direct preservation of the twining habit together with evidence of the dual-climbing phenomenon (Figure S2), indicating a high degree of ecological complexity in early Permian swamp forests. SUPPLEMENTAL INFORMATION Supplemental Information includes experimental procedures and two figures and can be found with this article online at https:// doi.org/10.1016/j.cub.2019.10.005. ACKNOWLEDGMENTS We are grateful to several technicians of NIGP, including Mei Shengwu, Mao Yongqiang, Yang Dinghua, Chen Youdong, Gao Yang,
Tang Jingjing and Zhang Xuansi for field and experimental assistance. This work is supported by the Strategic Priority Research Program (B) of CAS (XDB18000000, XDB26000000), the National Natural Science Foundation of China (41802011, 41872013, 41530101), the State Key Laboratory of Palaeobiology and Stratigraphy (NIGP) (20182114), the Visiting Professorship for Senior International Scientists of CAS (2016vea004) and the Grant Agency of Czech Republic (19-06728S). AUTHOR CONTRIBUTIONS W.Z. and J.W. designed the research. W.Z. and D.L. collected the specimens. W.Z. and C.K.B. prepared the manuscript. J.P. contributed the callistophytalean study. REFERENCES 1. Stein, W.E., Berry, C.M., Hernick, L.V., and Mannolini, F. (2012). Surprisingly complex community discovered in the mid-Devonian fossil forest at Gilboa. Nature 483, 78–81. 2. Xu, X.H., Berry, C.M., Wang, Y., and Marshall, J.E.A. (2011). A new species of Leclercqia Banks, Bonamo et Grierson (Lycopsida) from the middle Devonian of North Xinjiang, China, with a possible climbing habit. Int. J. Plant Sci. 172, 836–846. 3. Krings, M., Kerp, H., Taylor, T.N., and Taylor, T.E. (2003). How Paleozoic vines and lianas got off the ground: on scrambling and climbing Carboniferous–early Permian pteridosperms. Bot. Rev. 69, 204–224. 4. Burnham, R.J., (2009). An overview of the fossil record of climbers: bejucos, sogas, trepadoras, lianas, cipós, and vines. Revista Brasil. Paleontol. 12, 149–160. 5. DiMichele, W.A., and Falcon-Lang, H.J. (2011). Pennsylvanian ‘fossil forests’ in growth position (T0 assemblages): origin, taphonomic bias and palaeoecological insights. J. Geol. Soc. London 168, 585–605. 6. Wang, Q., Shen, S., and Li, Z.Y. (2013). A lefthanded, stem-twining plant from the Miocene Shanwang Formation of Eastern China. Am. J. Plant Sci. 4, 18–22. 7. Wang, J., Pfefferkorn, H.W., Zhang, Y., and Feng, Z. (2012). Permian vegetational Pompeii from Inner Mongolia and its implications for landscape paleoecology and paleobiogeography of Cathaysia. Proc. Natl. Acad. Sci. USA 109, 4927–4932. 8. Darwin, C. (1867). On the movements and habits of climbing plants. J. Linn. Soc. Lond. Bot. 9, 1–118. 9. Edwards, W., Moles, A.T., and Franks, P. (2007). The global trend in plant twining direction. Global Ecol. Biogeogr. 16, 795–800. 10. DiMichele, W.A., Phillips, T.L., and Pfefferkorn, H.W. (2006) Paleoecology of late Paleozoic pteridosperms from tropical Euramerica. J. Torrey Bot. Soc. 133, 83–118. 1 State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology and Center for Excellence in Life and Paleoenvironment, Chinese Academy of Sciences, Nanjing, China. 2University of Chinese Academy of Sciences, Beijing, China. 3Centre of Palaeobiodiversity, West Bohemian Museum in Pilsen, Pilsen, Czech Republic. 4Geological Sciences, Stanford University, Stanford, CA, USA. *E-mail: [email protected]
Current Biology 29, R1163–R1173, November 18, 2019 R1173