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Distinguishing Agromyzidae (Diptera) Leaf Mines in the Fossil Record

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Distinguishing Agromyzidae (Diptera) Leaf Mines in the Fossil Record Distinguishing Agromyzidae (Diptera) Leaf Mines in the Fossil Record: New Taxa from the Paleogene of North America and Germany and their Evolutionary Implications Author(s): Isaac S. Winkler, Conrad C. Labandeira, Torsten Wappler, and Peter Wilf Source: Journal of Paleontology, 84(5):935-954. 2010. Published By: The Paleontological Society DOI: http://dx.doi.org/10.1666/09-163.1 URL: http://www.bioone.org/doi/full/10.1666/09-163.1 BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. J. Paleont., 84(5), 2010, pp. 935–954 Copyright ’ 2010, The Paleontological Society 0022-3360/10/0084-0935$03.00 DISTINGUISHING AGROMYZIDAE (DIPTERA) LEAF MINES IN THE FOSSIL RECORD: NEW TAXA FROM THE PALEOGENE OF NORTH AMERICA AND GERMANY AND THEIR EVOLUTIONARY IMPLICATIONS ISAAC S. WINKLER,1,2 CONRAD C. LABANDEIRA,2,3 TORSTEN WAPPLER,4 AND PETER WILF5 1Department of Entomology, North Carolina State University, Raleigh, 27695-7613 USA, ,[email protected].; 2Department of Entomology, University of Maryland, College Park, 20742 USA; 3Department of Paleobiology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20213-7012 USA; 4Steinmann Institut fu¨r Geologie, Mineralogie, Pala¨ontologie, Universita¨t Bonn, Nussallee 8, D-53115 Bonn, Germany; and 5Department of Geosciences, Pennsylvania State University, University Park, 16802 USA ABSTRACT—Fossilized leaf mines and other traces of phytophagous insects provide a unique window into ecological and evolutionary associations of the past. Leaf-mining flies (Diptera: Agromyzidae) are an important component of the recent leaf-mining fauna, but their fossil record is sparse compared to other mining insect lineages; many putative agromyzid body fossils and traces are dubiously assigned. Agromyzid leaf mines often can be distinguished from those of other insects by the presence of an intermittent, fluidized frass trail that may alternate between the sides of the mine. Here, we describe two new Paleogene leaf mine fossils, Phytomyzites biliapchaensis Winkler, Labandeira and Wilf n. sp. from the early Paleocene of southeastern Montana, USA, occurring in leaves of Platanus raynoldsii (Platanaceae); and Phytomyzites schaarschmidti Wappler n. sp., from the middle Eocene of Messel, Germany, occurring in leaves of Toddalia ovata (Rutaceae). These fossils both exhibit frass trails indicative of an agromyzid origin, and P. biliapchaensis also exhibits associated stereotypical marks identical to damage caused by feeding punctures of extant adult female Agromyzidae prior to oviposition. Phytomyzites biliapchaensis represents the earliest confirmed record of Agromyzidae, and one of the earliest records for the large dipteran clade Schizophora. Plant hosts of both species belong to genera that are no longer hosts of leaf-mining Agromyzidae, suggesting a complex and dynamic history of early host-plant associations and, for the early Paleocene example, an evolutionary, possibly opportunistic colonization in the midst of the ecological chaos following the end-Cretaceous event in North America. INTRODUCTION name, larvae of most agromyzid flies are leaf-miners, but the OSSILIZED PLANT tissues containing distinctive insect- family includes some species that feed in stems, flower heads F feeding damage represent important evidence for inves- and seeds, roots, twig galls, and cambial or xylary tissues of tigating the ecology and evolution of ancient ecosystems arborescent plants. (Labandeira, 1998a, 2006; Wilf and Labandeira, 1999; The majority of extant agromyzid species are found on Zherikhin, 2002). Leaf mines, the traces of insect larvae herbaceous plants, but at least 40 extant species in eight genera feeding internally on leaf tissues typically beneath the mine leaves of arborescent species (Spencer, 1990). It appears epidermis, are common, and they have been reported that leaf-mining on trees has evolved several times within the repeatedly as fossils (Straus, 1977; Crane and Jarzembowski, Agromyzidae, but this trait is not characterized by a high 1980; Lang et al., 1995; Labandeira, 2002; Krassilov, 2008a). diversity of fly or host-plant species. In contrast, several In some cases, distinctive feeding patterns observed in fossil families of leaf-mining Lepidoptera are abundant and diverse leaf mines closely match those of extant taxa, in which case the on a wide variety of tree hosts, and less often attack fossils have important implications for the evolution of herbaceous plants (Connor and Taverner, 1997; Powell et specific insect groups (Opler, 1973; Labandeira et al., 1994, al., 1998). Leaf mines of lepidopterous origin are much more 1998b; Lopez-Vaamonde et al., 2006). However, taxonomic common than dipteran traces in the fossil record. This may be assignment of leaf mines can be problematic because insects largely attributable to the fact that leaves from large, from multiple orders and many families produce them, and persistent plants are much more likely to enter the fossil mine morphology may not be phylogenetically stable through record. Additionally, leaf mining is an ancient and common time (Grimaldi, 1999; Labandeira, 1998b, 2002a). Further- mode of life among early, basal families of Lepidoptera more, many characteristics of leaf mines, including overall (Labandeira et al., 1994; Powell et al., 1998). Because of this shape and pattern of frass deposition, often vary within historical incumbency and preference for woody plant hosts, a taxonomic groups and even among closely related species wide variety of leaf mines probably attributable to Lepidop- (Hering, 1957; Spencer, 1990). tera have been reported from the fossil record starting from Sixteen families of Diptera (true flies) include leaf- and the latest Early Cretaceous (Kozlov, 1988; Labandeira, 2006). stem- mining species, but these mostly belong to small groups Mines resembling those of the moth families Nepticulidae, a of miners in families with other predominant feeding habits relatively ancient leaf-mining lineage, and Gracillariidae are (Labandeira, 2005). The exception is the family Agromyzidae especially abundant and diverse in the fossil record (Opler, (leaf-mining flies), a large, diverse (2,800 spp.), and abundant 1973; Labandeira et al., 1994; Lang et al., 1995; Labandeira, group of internally-feeding phytophagous insects feeding on a 2002; Lopez-Vaamonde et al., 2006). wide variety of angiospermous plants (Spencer, 1990), as well Leaf-mining in the order Coleoptera (beetles) is of more as on a few non-angiosperms. As indicated by the common ancient origin; the earliest demonstrable leaf mine fossils— 935 936 JOURNAL OF PALEONTOLOGY, V. 84, NO. 5, 2010 from the Late Triassic of South Africa, Australia, and two other fossil species in Melanagromyza Hendel 1920 Kyrgyzstan (Rozefelds, 1985; Rozefelds and Sobbe, 1987; because of the visibly darkened haltere, a knob-like structure Zherikin, 2002; Scott et al., 2004)—may be attributable to this homologous to a reduced hind-wing in Diptera. This character order (Labandeira and Anderson, 2005; Labandeira, 2006a, is shared with several related genera now considered distinct 2006b). Beetle traces often resemble closely those of Lepidop- from Melanagromyza, and the pale-colored legs of M. tephrias tera, due to the similar form of the larval mouthparts. Melander, 1949, suggest that at least this species belongs to However, leaf-mining Coleoptera represent a small proportion another genus. Zlobin (2007) revisited previously described of extant leaf-mining taxa. Lastly, very rare mines attributable material from the Isle of Wight (Bembridge Marls, late to symphytan Hymenoptera have been noted in Paleogene Eocene) and noted specimens attributable by wing character- deposits (Wilf et al., 2006). istics to both extant subfamilies of Agromyzidae (Agromyzi- The fossil record of Agromyzidae is sparse and poorly nae and Phytomyzinae). However, poor preservation did not studied (Table 1), and many fossils have probably been allow generic assignment of these fossils. incorrectly referred to the family (Spencer and Martinez, Important evidence on the early evolution of Agromyzidae 1987). Although putative agromyzid mines have been reported is provided by a class of traces known as ‘‘Markflecke’’ or from the Paleocene (Crane and Jarzembowski, 1980), and even ‘‘pith flecks.’’ These are formed by the agromyzid genus from the Late Cretaceous (Turonian; Krassilov, 2007, 2008a, Phytobia Lioy, 1864, whose larvae bore in the cambium layer 2008b), until recently the earliest confirmable evidence of of trees, or just beneath in the layer of differentiating xylem agromyzid flies was from early middle Eocene borings
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