Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems
RESEARCH ARTICLE (Open Access)

New records of leaf galls and arthropod oviposition scars in Permian–Triassic Gondwanan gymnosperms

Stephen McLoughlin
+ Author Affiliations
- Author Affiliations

Department of Paleobotany, Swedish Museum of Natural History, Box 50007, SE-104 05, Stockholm, Sweden. Email: steve.mcloughlin@nrm.se

Australian Journal of Botany 59(2) 156-169 https://doi.org/10.1071/BT10297
Submitted: 8 November 2010  Accepted: 24 January 2011   Published: 28 March 2011

Abstract

Single, midrib-positioned galls and midrib-flanking oviposition scars are described from four species of Permian glossopterid foliage from Australia and South Africa. Several of these traces have been mistaken previously for glossopterid reproductive organs or fructification detachment scars. A single Early Triassic corystosperm leaf from Australia is reported bearing multiple disc-like galls on both the midrib and pinnules. A Middle Triassic taeniopterid gymnosperm leaf from Australia is described hosting oviposition scars between consecutive secondary veins flanking the midrib. These fossils attest to a much richer record of plant–arthropod interactions in the late Palaeozoic and early Mesozoic of high-latitude Gondwana than previously reported, and indicate that herbivory and reproductive strategies involving galling and foliar ovipositioning were re-established relatively soon after the end-Permian mass extinction event that saw major turnovers in both the flora and insect fauna.


References

Adami-Rodrigues K, Iannuzzi R, Pinto ID (2004) Permian plant–insect interactions from a Gondwana flora of southern Brazil. Fossils and Strata 51, 106–125.

Anderson JM, Anderson HM (1985) ‘Palaeoflora of southern Africa. Prodromus of South African megafloras Devonian to Lower Cretaceous.’ (A.A. Balkema: Rotterdam, The Netherlands)

Anderson JM, Anderson HM (1989) ‘Palaeoflora of southern Africa, Molteno Formation (Triassic) 2. Gymnosperms (excluding Dicroidium).’ (A.A. Balkema: Rotterdam, The Netherlands)

Anderson JM, Anderson HM, Archangelsky S, Bamford M, Chandra S, Dettmann ME, Hill RS, McLoughlin S, Rösler O (1999) Patterns of Gondwana plant colonisation and diversification. African Journal of Earth Sciences 28, 145–167.
Patterns of Gondwana plant colonisation and diversification.CrossRef |

Banerjee M (1969) Senotheca murulidihensis a new glossopteridean fructification from India associated with Glossopteris taeniopteroides Feistm. In ‘J. Sen memorial volume’. (Eds H Santapau, AK Ghosh, SK Roy, S Chanda, SK Choudhuri) pp. 359–368. (Botanical Society of Bengal: Calcutta, India)

Banerjee M, Bera S (1998) Record of zoocecidia on leaves of Glossopteris browniana Brongn. from Mohuda Basin, Upper Permian, Indian Lower Gondwana. Indian Biologist 30, 58–61.

Beattie R (2007) The geological setting and palaeoenvironmental and palaeoecological reconstructions of the Upper Permian insect beds at Belmont, New South Wales, Australia. African Invertebrates 48, 41–57.

Béthoux O, Galtier J, Nel A (2004) Earliest evidence of insect endophytic oviposition. Palaios 19, 408–413.
Earliest evidence of insect endophytic oviposition.CrossRef |

Bordy EM, Prevec R (2008) Sedimentology, palaeontology and palaeo-environments of the Middle (?) to Upper Permian Emakwenzini Formation (Karoo Supergroup, South Africa). South African Journal of Geology 111, 429–458.
Sedimentology, palaeontology and palaeo-environments of the Middle (?) to Upper Permian Emakwenzini Formation (Karoo Supergroup, South Africa).CrossRef |

Briggs DJC (1998) Permian Productidina and Strophalosiidina from the Sydney–Bowen Basin and New England Orogen: systematics and biostratigraphic significance. Memoir of the Association of Australasian Palaeontologists 19, 1–258.

Chin K (2007) The paleobiological implications of herbivorous dinosaur coprolites from the Upper Cretaceous Two Medicine Formation of Montana: why eat wood? Palaios 22, 554–566.
The paleobiological implications of herbivorous dinosaur coprolites from the Upper Cretaceous Two Medicine Formation of Montana: why eat wood?CrossRef |

Cuevas-Reyes P, Quesada M, Oyama K (2006) Abundance and leaf damage caused by gall-inducing insects in a Mexican tropical dry forest. Biotropica 38, 107–115.

Crespi BJ, Carmean DA, Chapman TW (1997) Ecology and evolution of galling thrips and their allies. Annual Review of Entomology 42, 51–71.
Ecology and evolution of galling thrips and their allies.CrossRef | 1:CAS:528:DyaK2sXjvFSgsw%3D%3D&md5=7ba5a7f9ab88a6ded5c364d084ff4918CAS | 15012307PubMed |

de Jersey NJ (1975) Miospore zones in the lower Mesozoic of southeastern Queensland. In ‘Gondwana geology: papers from the 3rd Gondwana symposium, Canberra, 1973’. (Ed. KSW Campbell) pp. 159–172. (ANU Press: Canberra)

Dreger-Jauffret F, Shorthouse JD (1992) Diversity of gall-inducing insects and their galls. In ‘Biology of insect-induced galls’. (Eds JD Shorthouse, O Rohfritsch) pp. 8–33. (Oxford University Press: Oxford, UK)

Erwin DH (2006) ‘Extinction. How life on Earth nearly ended 250 million years ago.’ (Princeton University Press: Princeton, NJ)

Gould RE, Delevoryas T (1977) The biology of Glossopteris: evidence from petrified seed-bearing and pollen-bearing organs. Alcheringa 1, 387–399.
The biology of Glossopteris: evidence from petrified seed-bearing and pollen-bearing organs.CrossRef |

Helby R, Morgan R, Partridge AD (1987) A palynological zonation of the Australian Mesozoic. Memoir of the Association of Australasian Palaeontologists 4, 1–94.

Karban R, Myers JH (1989) Induced plant responses to herbivory. Annual Review of Ecology and Systematics 20, 331–348.
Induced plant responses to herbivory.CrossRef |

Kellogg DW, Taylor EL (2004) Evidence of oribatid mite detritivory in Antarctica during the late Paleozoic and Mesozoic. Journal of Paleontology 78, 1146–1153.
Evidence of oribatid mite detritivory in Antarctica during the late Paleozoic and Mesozoic.CrossRef |

Keyser N (Compiler) (1997) ‘Geological map of the Republic of South Africa.’ (Council for Geoscience: Pretoria, South Africa)

Krassilov V, Silantieva N, Lewy Z (2008) Part I. Traumas on fossil leaves from the Cretaceous of Israel. In ‘Plant–arthropod interactions in the early angiosperm history. Evidence from the Cretaceous of Israel’. (Eds V Krassilov, A Rasnitsyn) pp. 1–187. (Pensoft Publishers: Sofia, Bulgaria)

Labandeira CC (1997) Insect mouthparts: ascertaining the paleobiology of insect feeding strategies. Annual Review of Ecology and Systematics 28, 153–193.
Insect mouthparts: ascertaining the paleobiology of insect feeding strategies.CrossRef |

Labandeira CC (2002) The history of associations between plants and animals. In ‘Plant–animal interactions: an evolutionary approach’. (Eds CM Herrera, O Pellmyr) pp. 26–74, 248–261. (Blackwell: London)

Labandeira CC (2005) The fossil record of insect extinction: new approaches and future directions. American Entomologist 51, 14–29.

Labandeira CC (2006) The four phases of plant-arthropod associations in deep time. Geologica Acta 4, 409–438.

Labandeira CC, Allen EG (2007) Minimal insect herbivory for the Lower Permian Coprolite Bone Bed site of north-central Texas, USA, and comparison to other late Paleozoic floras. Palaeogeography, Palaeoclimatology, Palaeoecology 247, 197–219.
Minimal insect herbivory for the Lower Permian Coprolite Bone Bed site of north-central Texas, USA, and comparison to other late Paleozoic floras.CrossRef |

Labandeira CC, Phillips TL (1996) A Carboniferous insect gall: insight into early ecologic history of the Holometabola. Proceedings of the National Academy of Sciences, USA 93, 8470–8474.
A Carboniferous insect gall: insight into early ecologic history of the Holometabola.CrossRef | 1:CAS:528:DyaK28XkvFyksb0%3D&md5=90ca22be4f02f1a3c81ac1d759d5a964CAS |

Labandeira CC, Phillips TL (2002) Stem borings and petiole galls from Pennsylvanian tree ferns of Illinois, USA: implications for the origin of the borer and galling functional-feeding-groups and holometabolous insects. Palaeontographica 264, 1–84.

Labandeira CC, Wilf P, Johnson KR, Marsh F (2007) ‘Guide to insect (and other) damage types on compressed plant fossils. Version 3.0.’ (Smithsonian Institution: Washington, DC)

Larew HG (1992) Fossil galls. In ‘Biology of insect-induced galls’. (Eds JD Shorthouse, O Rohfritsch) pp. 50–59. (Oxford University Press: New York)

Le Roux SF, Anderson HM (1977) A review of the localities and flora of the lowest Permian Karoo strata at Vereeniging, South Africa. Palaeontologia africana 20, 27–42.

Ludwig R (1857) Fossile Pflanzen aus der altestem Abtheilung der rheinisch-wetterauer Tertiär-Formation. Palaeontographica 8, 81–109.

Mani MS (1964) ‘Ecology of plant galls.’ (W. Junk: The Hague, The Netherlands)

Mani MS (1992) Introduction to Cecidology. In ‘Biology of insect-induced galls’. (Eds JD Shorthouse, O Rohfritsch) pp. 1–7. (Oxford University Press: Oxford, UK)

McLoughlin S (1988) Geology of the Inglis Dome, Denison Trough, central Queensland. Papers of the Department of Geology, University of Queensland 12, 229–263.

McLoughlin S (1990a) Some Permian glossopterid fructifications and leaves from the Bowen Basin, Queensland, Australia. Review of Palaeobotany and Palynology 62, 11–40.
Some Permian glossopterid fructifications and leaves from the Bowen Basin, Queensland, Australia.CrossRef |

McLoughlin S (1990b) Late Permian glossopterid fructifications from the Bowen and Sydney Basins, eastern Australia. Geobios 23, 283–297.
Late Permian glossopterid fructifications from the Bowen and Sydney Basins, eastern Australia.CrossRef |

McLoughlin S (1994a) Late Permian plant megafossils from the Bowen Basin, Queensland, Australia: Part 2. Palaeontographica (B) 231, 1–29.

McLoughlin S (1994b) Late Permian plant megafossils from the Bowen Basin, Queensland, Australia: Part 3. Palaeontographica (B) 231, 31–62.

Melville R (1983a) Two new genera of Glossopteridae. Botanical Journal of the Linnean Society 86, 275–277.
Two new genera of Glossopteridae.CrossRef |

Melville R (1983b) Glossopteridae, Angiospermidae and the evidence for angiosperm origins. Botanical Journal of the Linnean Society 86, 279–323.
Glossopteridae, Angiospermidae and the evidence for angiosperm origins.CrossRef |

Menendez CA (1962) Hallazgo de una fructificación en la Flora de Glossopteris de la provincia de Buenos Aires (Lanceolatus bonariensis sp. nov.). Con consideraciones sobre la nomenclatura de fructificaciones de Glossopteris. Ameghiniana 2, 175–182.

Meyer J (1987) ‘Plant galls and gall inducers.’ (Gebrüder Borntraeger: Berlin)

Millsteed BD (1994) Palynological evidence for the age of the Permian Karoo coal deposits near Vereeniging, northern Orange Free State, South Africa. South African Journal of Geology 97, 15–20.

Ogg JG, Ogg G, Gradstein FM (2008) ‘The concise geologic time scale.’ (Cambridge University Press: Cambridge, UK)

Pant DD, Srivastava PC (1995) Lower Gondwana insect remains and evidences of insect–plant interaction. In ‘Proceedings of the first international conference on global environment and diversification through geological time’. (Eds DD Pant, DD Nautiyal, AN Bhatnagar, KR Surange, MD Bose, PK Khare) pp. 317–326. (Society of Indian Plant Taxonomists: Allahabad, India)

Plumstead EP (1958) Further fructifications of the Glossopteridae and a provisional classification based on them. Transactions – Geological Society of South Africa 61, 1–58.

Plumstead EP (1962) Possible angiosperms from Lower Permian coal of the Transvaal. Nature 194, 594–595.
Possible angiosperms from Lower Permian coal of the Transvaal.CrossRef |

Plumstead EP (1963) The influence of plants and environment on the developing animal life of Karoo times. South African Journal of Science 59, 147–152.

Plumstead EP (1969) ‘Three thousand million years of plant life in Africa.’ Alex L Du Toit Memorial Lectures 11. (Geological Society of South Africa: Pretoria, South Africa)

Plumstead EP (1970) Recent progress and the future of palaeobotanical correlation in Gondwanaland. In ‘Proceedings 2nd IUGS symposium on Gondwana stratigraphy and palaeontology’. (Ed. SH Haughton) pp. 139–144. (Council for Scientific and Industrial Research, South Africa: Pretoria, South Africa)

Potonié H (1893) Die Flora des Rothliegenden von Thüringen. Abhandlungen der Koniglich Preussischen Geologischen Landesandstalt 9, 1–298.

Pott C, Labandeira CC, Krings M, Kerp H (2008) Fossil insect eggs and ovipositional damage on bennettitalean leaf cuticles from the Carnian (Upper Triassic) of Austria. Journal of Paleontology 82, 778–789.
Fossil insect eggs and ovipositional damage on bennettitalean leaf cuticles from the Carnian (Upper Triassic) of Austria.CrossRef |

Prevec R, Labandeira CC, Neveling J, Gastaldo RA, Looy CV, Bamford M (2009) Portrait of a Gondwanan ecosystem: a new late Permian fossil locality from KwaZulu-Natal, South Africa. Review of Palaeobotany and Palynology 156, 454–493.
Portrait of a Gondwanan ecosystem: a new late Permian fossil locality from KwaZulu-Natal, South Africa.CrossRef |

Price PL (1983) A Permian palynostratigraphy for Queensland. In ‘Proceedings of the symposium on the Permian geology of Queensland’. (Ed. Anonymous) pp. 155–212. (Geological Society of Australia, Queensland Division: Brisbane)

Raman A, Schaefer CW, Withers TM (2005) Galls and gall-inducing arthropods: an overview of their biology, ecology, and evolution. In ‘Biology, ecology, and evolution of gall-inducing arthropods’. (Eds A Raman, CW Schaefer, TM Withers) pp. 1–33. (Science Publishers Inc.: Enfield, NH)

Retallack GJ (1977) Reconstructing Triassic vegetation of eastern Australasia: a new approach for the biostratigraphy of Gondwanaland. Alcheringa 1, 247–278.
Reconstructing Triassic vegetation of eastern Australasia: a new approach for the biostratigraphy of Gondwanaland.CrossRef |

Retallack GJ (1980) Late Carboniferous to Middle Triassic megafossil floras from the Sydney Basin. In ‘A guide to the Sydney Basin’. (Eds C Herbert, RJ Helby) pp. 384–430. (Geological Survey of NSW Bulletin 26: Sydney)

Rohfritsch O (2008) Plants, gall midges, and fungi: a three-component system. Entomologia Experimentalis et Applicata 128, 208–216.
Plants, gall midges, and fungi: a three-component system.CrossRef |

Roskam JC (1992) Evolution of the gall-inducing guild. In ‘Biology of insect-induced galls’. (Eds JD Shorthouse, O Rohfritsch) pp. 34–49. (Oxford University Press: Oxford, UK)

Rozefelds AC, Sobbe I (1987) Problematic insect leaf mines from the Upper Triassic Ipswich Coal Measures of southeastern Queensland, Australia. Alcheringa 11, 51–57.
Problematic insect leaf mines from the Upper Triassic Ipswich Coal Measures of southeastern Queensland, Australia.CrossRef |

Sarzetti LC, Labandeira CC, Muzón J, Wilf P, Cúneo NR, Johnson KR, Genise JF (2009) Odonatan endophytic oviposition from the Eocene of Patagonia: the ichnogenus Paleoovoidus and implications for behavioral stasis. Journal of Paleontology 83, 431–447.
Odonatan endophytic oviposition from the Eocene of Patagonia: the ichnogenus Paleoovoidus and implications for behavioral stasis.CrossRef |

Scotese CR (1997) ‘Paleogeographic atlas. PALEOMAP progress report 90-0497.’ (Department of Geology, University of Texas: Arlington, TX)

Scott AC, Stephenson J, Collinson ME (1994) The fossil record of plant galls. In ‘Plant galls: organisms, interactions, populations’. (Ed. MAJ Williams) pp. 447–470. (Systematics Association Special Volume 49, Clarendon Press: Oxford, UK)

Scott AC, Anderson JM, Anderson HM (2004) Evidence of plant–insect interactions in the Upper Triassic Molteno Formation of South Africa. Journal of the Geological Society 161, 401–410.

Sen J (1955) On some fructifications borne on Glossopteris leaves. Botaniska Notiser 108, 245–251.

Sen J (1963) A glossopteridean fructification from India. Nature 200, 1124
A glossopteridean fructification from India.CrossRef | 14098462PubMed |

Shi GR, Waterhouse JB, McLoughlin S (2010) The Lopingian of Australasia: a review of biostratigraphy, correlations, palaeogeography and palaeobiogeography. Geological Journal 45, 230–263.
The Lopingian of Australasia: a review of biostratigraphy, correlations, palaeogeography and palaeobiogeography.CrossRef |

Shorthouse JD, Wool D, Raman A (2005) Gall-inducing insects – Nature’s most sophisticated herbivores. Basic and Applied Ecology 6, 407–411.
Gall-inducing insects – Nature’s most sophisticated herbivores.CrossRef |

Silva IM, Andrade GI, Fernandes GW, Lemos Filho JP (1996) Parasitic relationships between a gall-forming insect Tomoplagia rudolphi (Diptera: Tephritidae) and its host plant (Vernonia polyanthes, Asteraceae). Annals of Botany 78, 45–48.
Parasitic relationships between a gall-forming insect Tomoplagia rudolphi (Diptera: Tephritidae) and its host plant (Vernonia polyanthes, Asteraceae).CrossRef |

Singh SM (2002) Seeds, fructifications, bracts and calamitalean axes from the Karanpura and Bokaro group of coalfields. The Palaeobotanist 51, 73–79.

Srivastava PN (1956) Studies in the Glossopteris flora of India – 4. Glossopteris, Gangamopteris and Palaeovittaria from the Raniganj Coalfield. The Palaeobotanist 5, 1–45.

Tadros NZ (1995) Sydney–Gunnedah Basin overview. In ‘Geology of Australian coal basins’. (Eds CR Ward, HJ Harrington, CW Mallett, JW Beeston) pp. 163–175. (Geological Society of Australia, Coal Geology Group, Special Publication 1: Sydney)

Teaford MF (1991) Dental microwear: what can it tell us about diet and dental function? In ‘Advances in dental anthropology’. (Eds MA Larsen, CS Kelley) pp. 341–356. (Alan R. Liss: New York)

Tosolini A-MP, Pole M (2010) Insect and clitellate annelid traces in mesofossil assemblages from the Cretaceous of Australasia. Alcheringa 34, 397–419.
Insect and clitellate annelid traces in mesofossil assemblages from the Cretaceous of Australasia.CrossRef |

van Amerom HWJ (1973) Gibt es Cecidien im Karbon bei Calamiten und Asterophylliten? In ‘Compte rendu septième congrès international de stratigraphie et de géologie du carbonifère’. (Ed. K-H Josten) pp. 63–83. (Van Acken: Krefeld, Germany)

Vijaya , Prasad GVR, Singh K (2009) Late Triassic palynoflora from the Pranhita–Godavari Valley, India: evidence from vertebrate coprolites. Alcheringa 33, 91–111.
Late Triassic palynoflora from the Pranhita–Godavari Valley, India: evidence from vertebrate coprolites.CrossRef |

Vjalov OS (1975) Fossil remains of insect feeding. Paleontologicheskiy Sbornik 1–2, 147–155.

Wappler T, Ben-Dov Y (2008) Preservation of armoured scale insects on angiosperm leaves from the Eocene of Germany. Acta Palaeontologica Polonica 53, 627–634.
Preservation of armoured scale insects on angiosperm leaves from the Eocene of Germany.CrossRef |

Weaver L, McLoughlin S, Drinnan AN (1997) Fossil woods from the Upper Permian Bainmedart Coal Measures, northern Prince Charles Mountains, East Antarctica. AGSO Journal of Australian Geology & Geophysics 16, 655–676.

Webb JA (1982a) Triassic radiometric dates from eastern Australia. In ‘Numerical dating in stratigraphy’. (Ed. GS Odin) pp. 515–521. (John Wiley: New York)

Webb JA (1982b) Triassic species of Dictyophyllum from eastern Australia. AIcheringa 6, 79–91.
Triassic species of Dictyophyllum from eastern Australia.CrossRef |

White ME (1961) Permian plant fossils from the Agate Creek Volcanics, north Queensland. Bureau of Mineral Resources, Geology and Geophysics, Australia Record 1961(20), 1–10. [unpublished; available from Geoscience Australia: http://www.ga.gov.au/].

Whitham TG (1978) Habitat selection by Pemphigus aphids in response to resource limitation and competition. Ecology 59, 1164–1176.
Habitat selection by Pemphigus aphids in response to resource limitation and competition.CrossRef |

Williams AG, Whitham TG (1986) Premature leaf abscission: an induced plant defense against gall aphids. Ecology 67, 1619–1627.
Premature leaf abscission: an induced plant defense against gall aphids.CrossRef |

Wool D (1984) Gall-forming aphids. In ‘The biology of gall insects’. (Ed. TN Ananthakrishnan) pp. 11–58. (Edward Arnold: New Delhi, India)

Yoo EK, Norman A, McDonald I (1995) Sydney Basin – Western Coalfied. In ‘Geology of Australian coal basins’. (Eds CR Ward, HJ Harrington, CW Mallett, JW Beeston) pp. 231–245. Coal Geology Group, Special Publication 1. (Geological Society of Australia: Sydney)


Full Text PDF (3.8 MB) Export Citation Cited By (29)

View Altmetrics