J. Paleont., 83(3), 2009, pp. 431–447 Copyright ᭧ 2009, The Paleontological Society 0022-3360/09/0083-431$03.00

ODONATAN ENDOPHYTIC OVIPOSITION FROM THE EOCENE OF PATAGONIA: THE ICHNOGENUS PALEOOVOIDUS AND IMPLICATIONS FOR BEHAVIORAL STASIS

LAURA C. SARZETTI,1 CONRAD C. LABANDEIRA,2,3 JAVIER MUZO´ N,4 PETER WILF,5 N. RUBE´ NCU´ NEO,1 KIRK R. JOHNSON,6 AND JORGE F. GENISE1 1CONICET, Museo Paleontolo´gico Egidio Feruglio, Avenida Fontana 140, Trelew, Chubut 9100, Argentina, Ͻ[email protected]Ͼ, Ͻ[email protected]Ͼ and Ͻ[email protected]Ͼ; 2Department of Paleobiology, National Museum of Natural History, Smithsonian Institution, 20213-7012; 3Department of Entomology, University of Maryland, College Park, Maryland 20742, Ͻ[email protected]Ͼ; 4Instituto de Limnologı´a ‘‘Dr. Raul A. Ringuelet,’’ Av. Calchaquı´ Km 23,5 712, Florencio Varela, Buenos Aires, Argentina, 1888, Ͻ[email protected]Ͼ; 5Department of Geosciences, Pennsylvania State University, University Park, Pennsylvania, 16802, Ͻ[email protected]Ͼ; and 6Department of Earth Sciences, Denver Museum of Nature and Science, Denver, Colorado 80205, Ͻ[email protected]Ͼ

ABSTRACT—We document evidence of endophytic oviposition on fossil compression/impression leaves from the early Eocene Laguna del Hunco and middle Eocene Rı´o Pichileufu´ floras of Patagonia, Argentina. Based on distinctive mor- phologies and damage patterns of elongate, ovoid, lens-, or teardrop-shaped scars in the leaves, we assign this insect damage to the ichnogenus Paleoovoidus, consisting of an existing ichnospecies, P. rectus, and two new ichnospecies, P. arcuatum and P. bifurcatus.InP. rectus, the scars are characteristically arranged in linear rows along the midvein; in P. bifurcatus, scars are distributed in double rows along the midvein and parallel to secondary veins; and in P. arcuatum, scars are deployed in rectilinear and arcuate rows. In some cases, the narrow, angulate end of individual scars bear a darkened region encompassing a circular hole or similar feature indicating ovipositor tissue penetration. A comparison to the structure and surface pattern of modern ovipositional damage on dicotyledonous leaves suggests considerable similarity to certain zygopteran Odonata. Specifically, members of the Lestidae probably produced P. rectus and P. bifurcatus, whereas species of Coenagrionidae were responsible for P. arcuatum. Both Patagonian localities represent an elevated diversity of potential fern, gymnosperm, and especially angiosperm hosts, the targets of all observed oviposition. However, we did not detect targeting of particular plant families. Our results indicate behavioral stasis for the three ovipositional patterns for at least 50 million years. Nevertheless, synonymy of these oviposition patterns with mid- Mesozoic ichnospecies indicates older origins for these distinctive modes of oviposition.

INTRODUCTION 1991; Labandeira, 2002a, 2002b) and Spain (Pen˜alver and Del- VIPOSITION ON vegetation is a common insect behavior, in clo`s, 2004), from the Oligocene of Germany (Hellmund and Hell- O which eggs are deposited either on the surfaces of plant mund, 1991, 1993, 1996a, 1996b, 1998, 2002b; Van Konijnen- organs (exophytic oviposition) or, alternatively, inserted within burg-van Cittert and Schemießner, 1999), and from the early and plant tissues (endophytic oviposition; Corbet, 1999). Endophytic late Miocene of Germany (Hellmund and Hellmund, 1996c, oviposition represents an ancient behavior, based on external ovi- 2002a, 2002c). positor structure found in some Paleozoic insects (Carpenter, Complex patterns of ovipositional plant damage frequently al- 1971; Labandeira, 1998) and additionally on stereotyped tissue low reliable identification of the producers, particularly when fos- sil ovipositor structure and egg-laying biology of modern coun- damage occurring within foliage and stems (Labandeira, 2002b; terparts are well studied. Accordingly, most post-Paleozoic fossil Be´thoux et al., 2004, Beattie, 2007). Externally evident, often occurrences of oviposition are confidently attributed to the Odon- sawlike ovipositors have been recognized in the Palaeodictyop- ata (Hellmund and Hellmund, 1991; Grauvogel-Stamm and Kel- tera, Protodonata, Dictyoptera, Archaeorthoptera, Hemipteroidea, ber, 1996; Van Konijnenburg-van Cittert and Schemießner, 1999; and early-derived holometabolous clades from the Late Carbon- Labandeira, 2002a, 2002b; Adami-Rodrigues et al., 2004; Pen˜al- iferous through the Triassic (Labandeira, 2006). External ovipos- ver and Delclo`s, 2004; Gnaedinger et al., 2007), including those itors currently are most prominent in the orders Odonata, Orthop- described below. tera, Hemiptera, Coleoptera, Lepidoptera and Hymenoptera (Zeh Despite the extensive fossil evidence, as well as autecological et al., 1989). knowledge of modern ovipositing insects (Wesenberg-Lund, Worldwide, evidence for leaf damage produced by ovipositors 1913b; Schiemenz, 1957; Corbet, 1999), formal ichnotaxonomic is relatively abundant throughout the Phanerozoic. Several Paleo- treatments of these trace fossils were lacking until Vasilenko zoic examples have been documented on sphenopsid stems from (2005) established the ichnogenus Paleoovoidus, the first ichno- the Late Pennsylvanian of France (Be´thoux et al., 2004) and the taxon created for ovipositional damage to fossil plants. In a more Middle Permian of Germany (Roselt, 1954), and especially on recent and extensive documentation, Krassilov and Silantieva glossopterid leaves from the Late Permian of Australia (Beattie, (2008) defined several new ichnogenera and ichnospecies to in- 2007), South Africa (Prevec et al., 2009), India (Bunbury, 1861; clude oviposition scars and presumably arthropod eggs from the Banerji, 2004), and Brazil (Adami-Rodrigues et al., 2004). For Late Cretaceous (Turonian) Gerofit locality in Israel. Recently, the Mesozoic, oviposition has been recorded for a variety of sphe- Vasilenko (2008) redefined their ichnogenus Paleoovoidus and nopsids and seed plants from the Middle and Late Triassic of also described two new ichnospecies, P. flabellatus and P. arcu- Germany and France (Kelber, 1988; Grauvogel-Stamm and Kel- atus, assigning them to endophytic ovipositional traces. He ad- ber, 1996), Chile (Gnaedinger et al., 2007) and Austria (Pott et ditionally defined a new ichnogenus, Palaexovoidus, to refer to al., 2007); the Early Jurassic of Germany (Van Konijnenburg-van exophytic oviposition on plant tissues. Before the establishment Cittert and Schmeinßner, 1999); and the early Late Cretaceous of of these taxa, trace fossils of oviposition in leaves and stems were Israel (Krassilov et al., 2007) and Germany (Hellmund and Hell- described in the literature without formal ichnotaxonomic analy- mund, 1996c). Cenozoic occurrences are known from the Eocene ses (e.g., Hellmund and Hellmund, 1998; Labandeira, 2002a), in- for Washington State in the United States (Lewis and Carroll, cluding the damage-type (DT) system of Labandeira et al. (2007), 431 432 JOURNAL OF PALEONTOLOGY, V. 83, NO. 3, 2009

al., 2005b), including oviposition, which was mentioned but not analyzed by Wilf et al. (2005b). The Laguna del Hunco (LH) paleoflora comes from a caldera- lake deposit, the Tufolitas Laguna del Hunco (Arago´n and Maz- zoni, 1997; Arago´n et al., 2001), and is located in western Chubut Province, Argentina, 160 km southeast from the Rı´o Pichileufu´ (RP) locality, along the foothills of the Sierra de Huancache at S42.5, W70.0 degrees (Fig. 1). The fossil material originates from strata consisting of tuffaceous mudstones and sandstones, inter- preted as a caldera-collapse lake unit within the expansive middle Chubut River volcanic-pyroclastic complex (Arago´n and Romero, 1984; Arago´n and Mazzoni, 1997). The entombed plant remains are preserved principally as impressions; angiosperm leaf impres- sions are the most abundant plant organs, though there are also significant gymnosperm and minor fern components (Wilf et al., 2005a). Recently, 25 distinct fossil plant localities (known as LH1-25) were intensively collected and placed in a 170 m measured strati- graphic section, from which six paleomagnetic reversals were de- tected, and three tuffs interbedded with the fossils were dated using the 40Ar-39Ar method (Wilf et al., 2003). All Ar-Ar ages were near 52 Ma; and one tuff containing sanidine was reana- lyzed, yielding an age of 51.91 Ϯ 0.22 Ma (Wilf et al., 2005a). The combined evidence placed the LH flora within the sustained period of globally warm temperatures known as the early Eocene climatic optimum (Zachos et al., 2001). Leaf-margin and leaf-area analyses indicate local mean-annual paleotemperatures near 16.6 ЊC and annual rainfall of at least 1140 mm, though certain plant taxa suggest much higher rainfall (Wilf et al., 2005a, 2008). A number of botanical investigations have emerged from the recent collecting effort, which has yielded Ͼ210 species, including stud- ies of Myrtaceae (Gandolfo et al., 2006), Casuarinaceae (Zamaloa FIGURE 1—Map of central Patagonia showing 50 Ma positions of both et al., 2006), Proteaceae (Gonza´lez et al., 2007), and many other localities under study, with modern coastlines: Laguna del Hunco (Chubut Province) and Rı´o Pichileufu´ (Rı´o Negro Province) (redrawn from Wilf et al., groups (Wilf et al., 2007). 2005). Several entomological studies have revealed the presence of a diverse insect fauna, including representatives of the orders Odon- ata, Blattodea, Orthoptera, Hemiptera, Coleoptera, Mecoptera, Diptera, Hymenoptera and Trichoptera (Rossi de Garcı´a, 1983; used for analyzing the paleoecology of plant-insect associational Petrulevicˇius and Martins-Neto, 2000; Genise and Petrulevicˇius, patterns. Additionally, erection of ichnotaxa for ovipositional 2001; Petrulevicˇius and Nel, 2003a; Petrulevicˇius, 2005). Addi- trace fossils was not considered in several more encompassing tionally, pipoid anurans were described by Casamiquela (1961) studies (Van Amerom, 1966; Straus, 1977; Givulescu, 1984; Vas- and Ba´ez and Trueb (1997) and a catfish species by Sa´ez (1941). ilenko, 2006, 2007), whereas in most of those same works, nu- Nevertheless, the preserved fauna is less abundant and diverse merous ichnotaxa were established for various other types of fo- than the flora of this locality, though insect damage to fossil liar damage. leaves is abundant and extremely diverse (Wilf et al., 2005b). This contribution has three principal objectives. The first is to The Rı´o Pichileufu´ (RP) paleoflora originates from a probable formally define new ichnospecies and to provide additional evi- caldera-lake facies of the Ventana Formation (Arago´n and Ro- dence for previously defined ovipositional damage from two di- mero, 1984) and is located in Rı´o Negro Province of Argentina, verse Eocene Patagonian paleofloras. Establishment of these new approximately 40 km east from the city of San Carlos de Bari- ichnotaxa will be done by comparison with analogous oviposi- loche at S41.2, W70.8 degrees (Fig. 1). The RP flora was the tional damage by modern Odonata. The second is to ascertain subject of an early monograph (Berry, 1938) that remains the whether the ichnotaxa from these Eocene paleofloras have other most extensive on Cenozoic macrofloras in South America, occurrences in the fossil record, providing a brief review of the though nearly all taxa are in need of revision. More recently, the relevant fossil record of endophytic oviposition in leaves. The flora was extensively recollected from three quarries (known as third is to track long-term ovipositional behavior of odonatan lin- RP1-3), and tuffs immediately associated with the fossil floras eages inflicted on leaves about 50 million years ago, comparing produced an Ar-Ar age of 47.46 Ϯ 0.05 Ma (Wilf et al., 2005a). these oviposition patterns with earlier occurrences of the ichno- There is much less fossiliferous exposure at RP than at LH, and taxa. preservation is not as good, but the floral diversity at RP3 is similar to that of the richest LH quarries (Wilf et al., 2005a). Like GEOLOGICAL SETTING LH, the RP flora is dominated by angiosperm leaves but has sig- Leaves bearing oviposition scars analyzed in this contribution nificant contributions from gymnosperms such as Araucaria, Po- originate from the Laguna del Hunco (early Eocene, 51.91 Ϯ 0.22 docarpaceae, and Ginkgo, as well as fern species. Early studies Ma) and Rı´o Pichileufu´ (middle Eocene, 47.46 Ϯ 0.05 Ma) sites of this locality (Berry, 1935a, 1935b, 1938) revealed a great di- in central Patagonia (Fig. 1; Wilf et al., 2005a). These two classic versity of fossil plant taxa that are only recently being taxonom- paleobotanical localities (Berry, 1925, 1928, 1935a, 1935b, ically updated. Based on preliminary leaf-margin analysis, the RP 1935c; Frenguelli, 1943a, 1943b; Romero and Hickey, 1976; Gan- mean annual paleotemperature is 19.2 Ϯ 2.4 ЊC (Wilf et al., dolfo et al., 1988), exhibit very diverse paleofloras (Wilf et al., 2005a). 2005a) and associated spectra of insect-mediated damage (Wilf et Fossil frogs and insects, including large ants, have been noted SARZETTI ET AL.—EOCENE ODONATAN OVIPOSITION FROM PATAGONIA 433

FIGURE 2—1, Paleoovoidus bifurcatus, isp. nov., holotype specimen (MPEF-IC-1385) on a sapindaceous leaf (LH13, morphotype indeterminate, MPEF- Pb-1607), scale bar: 0. 5 cm; 2, specimen MPEF-IC-1385 enlarged from boxed area in A of Paleoovoidus bifurcatus, scale bar: 1 mm; 3, Paleoovoidus rectus specimen (MPEF-IC-1376) on ‘‘Myrcia’’ chubutensis (LH13, morphotype TY21, MPEF-Pb-2216), enlarged from boxed area in D, scale bar: 0. 5 cm; 4, specimen MPEF-IC showing P. rectus (boxed area) and P. arcuatum below (MPEF-IC 1392).

from the plant-bearing beds (Wilf et al., 2005a), although Archi- SYSTEMATIC ICHNOLOGY myrmex piatnitzkyi, reported from the general area (Viana and The specimens described here are deposited in the Museo Pa- Haedo-Rossi, 1957; Dlussky and Perfilieva, 2003), can not be leontolo´gico Egidio Feruglio, Trelew, Chubut, under the paleo- correlated stratigraphically to the flora as suggested by those au- botanical collections (MPEF-Pb, for the leaf holding the trace), thors, due to local faulting (Wilf and Johnson, personal observa- with each trace assigned to a separate suite of ichnological col- tion, 2008). Also leaf-cutter bee (Megachilidae) foliar damage lection numbers (MPEF-IC). was reported from RP (Sarzetti et al., 2008). Interestingly, Berry (1938) figured an extensively insect-damaged leaf from RP he Ichnogenus PALEOOVOIDUS Vasilenko, 2005 Anona infestans named ‘‘ ’’ , one of the earliest explicit illustrations Figure 2 of fossil insect damage from South America. Berry (1938, p.73) reported that the damage ‘‘might be the remains of scale insects.’’ Paleoovoidus VASILENKO, 2005, p. 630, figs. 1–3. Our updated interpretation of this damage as oviposition scars Sertoveon KRASSILOV, 2008, partim, p. 69, figs. 1–5. appears below. Paleoovoidus VASILENKO, 2008, p. 516, fig. 2, pl. 7. 434 JOURNAL OF PALEONTOLOGY, V. 83, NO. 3, 2009 SARZETTI ET AL.—EOCENE ODONATAN OVIPOSITION FROM PATAGONIA 435

FIGURE 4—Camera lucida drawing of a specimen of Paleoovoidus arcuatum, isp. nov. (MPEF-IC-1370), on the dicot ‘‘Celtis’’ ameghenoi (LH2, morphotype ?TY20, MPEF-Pb-1053), scale bar: 1 cm: 1, entire specimen, show a register of five rows of oviposition scars oriented across the blade from upper-left to the center, and a differently juxtaposed register of perhaps five rows at the upper-right region of the leaf; 2, minor enlargement of six scars with central ovoidal depressions from a circled region of the leaf margin at upper-left; 3, major enlargement of callus and emergence hole detail from a single scar, indicated by a circular template from the leaf margin at center-left; 4, similar enlargement of three scars with central emergence holes, from the circled leaf region at center-bottom, axial length of leaf: 4.5 cm, scale bar as in Fig. 3.5.

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FIGURE 3—Paleoovoidus arcuatum specimens: 1, MPEF-IC-1380a, MPEF-IC-1380b and MPEF-IC-1380c specimens on an unknown dicot leaf (LH13, morphotype indeterminate, MPEF-Pb-1591), showing a zigzag pattern, lettered arrows point to individual rows or ‘‘files’’ of oviposition marks; 2, MPEF-IC- 1371a-c showing consecutive and parallel rows on an indeterminate dicot leaf (LH6, morphotype indeterminate, MPEF-Pb-1054), scale bar: 1 cm; 3, linear oviposition arcs (lettered arrows) covering MPEF-IC-1374a and specimens MPEF-IC-1374b, c on ‘‘Cupania’’ latifolioides (LH18, ?Cunoniaceae, MPEF-Pb- 1585), scale bar: 1 cm; 4, trace-fossil specimens MPEF-IC-1388 a-e (lettered lines) on an indeterminate dicot leaf (RP3, morphotype indeterminate, MPEF- Pb-1611), scale bar: 1 cm; 5, specimens MPEF-IC-1370 a-g (lettered lines) on the dicot ‘‘Celtis’’ ameghenoi (LH2, morphotype TY20, MPEF-Pb 1053), scale bar: 1 cm. 436 JOURNAL OF PALEONTOLOGY, V. 83, NO. 3, 2009 SARZETTI ET AL.—EOCENE ODONATAN OVIPOSITION FROM PATAGONIA 437

‘‘Flea beetle egg deposition,’’ LEWIS AND CARROLL, 1991, p. 335, and they lack the dark spot observed in other specimens. In ad- fig. 2. dition, we note that in this leaf a distinctive occurrence of Pa- ‘‘Flea beetle egg deposition,’’ LEWIS AND CARROLL, 1992, p. 3, leoovoidus arcuatum (MPEF-IC 1392) (Fig. 2.3) appears basal to fig. 2. the P. rectus trace, indicating that both patterns can occur on the Emended diagnosis.⎯Medium-sized elongate, narrow, ovoid, same leaf. or lens-shaped structures, characterized by regular arrangement in The P. rectus holotype described by Vasilenko (2005) exhibits leaf lamina. These structures, defined by dark, surrounding reac- minor differences from the material presented here. Vasilenko’s tion tissue, are narrow at one end, each of which often bears a (2005) oviposition damage has a similar arrangement, orientation, dark spot. and measurements compared with the LH specimen, but the scars Discussion.⎯Vasilenko (2005, p. 629) erected the ichnogenus are distributed in two linear rows adjacent to the central vein in Paleoovoidus originally as ‘‘oval or lentiform structures (eggs) Pityophyllum sp. leaves (Coniferales: Pinaceae), and in up to four with regular distribution over substrate.’’ More recently, Vasilen- subparallel rows on Ginkgoites (Ginkgoales: Ginkgoaceae), which ko (2008) redefined the ichnogenus, providing a more precise lack a midvein. None of these scars occurs within veins. Our LH diagnosis. Nevertheless, the diagnosis is emended here because specimen also resembles the Lower Jurassic scar pattern docu- we consider that the term ‘‘substrate’’ should be restricted to mented by Van Konijnenburg-van Cittert and Schmeißner (1999) leaves, which probably was the original intention of the author. in leaves of Schmeissneria microstachys (Ginkgoales: Schmeis- In addition, the mention of ‘‘eggs’’ in the diagnosis is dispensed sneriaceae) and Podozamites distans (Coniferales: Podocarpa- with herein, as there is no indication for the presence of eggs, ceae); both species lack midveins. These authors described two thus rendering moot the author’s inference. Alternatively, Kras- types of row arrangement, but in both cases, the scars are slightly silov and Silantieva (2008) defined the ichnogenus Sertoveon to longer than the Patagonian material, with major-axis values ap- correspond with a structure and distribution over the leaf lamina proximating 3 mm. These multiple rows provide the most impor- very similar to our material. However, according to the current tant difference from the pattern described here, where scars are rules of zoological nomenclature, the valid name should be Pa- distributed along a single row. leoovoidus because of date priority over Sertoveon. Other ich- Material examined.⎯One specimen (MPEF-IC-1376) occurs nogenera erected by Krassilov and Silantieva (2008), Costoveon on a ‘‘Myrcia’’ chubutensis (MPEF-Pb-2216, from locality LH13 and Catenoveon, are comparable with Paleoovoidus, although the of Wilf et al., 2003), from the early Eocene Tufolitas Laguna del disposition of the scars over the leaf are different. In Costoveon, Hunco, Chubut Province, Argentina (Fig. 2.3). all scars are distributed over primary veins. By contrast, Caten- Discussion.⎯Vasilenko (2005) defined this ichnospecies as oveon is similar to Paleoovoidus in that the scars are oriented in ‘‘oval or lentiform relief structures, individual eggs oriented in the direction of stronger veins, but the sets of scars cover the chain on leaf blades.’’ The diagnosis is emended here to avoid entire surface of the lamina. the use of an interpretative concept, such as ‘‘eggs’’ and to pro- vide a more accurate description of the oviposition pattern. How- PALEOOVOIDUS RECTUS Vasilenko, 2005 ever, Pott et al. (2008) have described Late Triassic oviposition Figure 2.2, 2.4 scars from Austria with preserved ovoidal egg cuticles in ben- ‘‘Odonata eggs’’ VAN KONIJNENBURG-VAN CITTERT AND nettitalean leaves, arranged in a near-circular pattern but lacking SCHMEIßNER, 1999, p. 217. the linearity of P. rectus. These early Mesozoic ichnospecies can ‘‘Egg scars’’ KRASSILOV,SILANTIEVA,HELLMUND, AND HELL- be distinguished from the ichnospecies P. rectus because of the MUND, 2007, p. 806, fig. 3D. arrangement of scars in a single row. Krassilov and Silantieva Emended diagnosis.⎯Elongate to lens-shaped scars oriented in (2008) defined a similar ichnospecies, Catenoveon undulatum. a single, linear row, with long axes of scars aligned lengthwise, However, their definition included ‘‘elliptical to fusiform egg mostly parallel to the long axis of the leaf and usually occurring pits’’ (page 68) distributed nearly parallel or oblique to veins but along the midrib. distributed over most of the leaf. The principal difference between Description.⎯The specimen of Paleoovoidus rectus (Fig. 2.3) C. undulatum and P. rectus is that oviposition scars cover most occurs in a leaf of ‘‘Myrcia’’ chubutensis (Myrtaceae, MPEF-Pb of the laminar surface, whereas in P. rectus a single linear row 2216). This leaf has two sets of leaf scars; those corresponding is present along the primary vein. We consider Vasilenkos ich- to C. rectus are indicated by the inset box in Figure. 2.4. There nospecies Paleoovoidus rectus (2005) more germane for under- are twelve scars arranged rectilinearly near the leaf apex, aligned standing the pattern in the Patagonian specimen. Other similar approximately along the primary vein, with the scar long axis evidence of P. rectus comes from the Mesozoic (Van Konijnen- parallel or subparallel to the vein. Two scars are on the primary burg-van Cittert, 1999; Vasilenko, 2005). These occurrences ap- vein, whereas the other ten are closely adjacent to it in a single pear to be associated with the great diversity of parallel-veined, row along the intersection of the laminar and veinal tissue, except broadleaved gymnosperms from floras of Late Triassic to Early for the two closest scars at the tip of the leaf that appear on the Cretaceous age. Older documentation comes from Late Permian opposite side of the primary vein. The individual length of the floras, typically occurring in or adjacent to the robust midribs of scars ranges from 1.0 to 1.2 mm, and the width ranges from 0.4 Glossopteris leaves. Paleozoic occurrences were probably pro- to 0.5 mm. The distance between adjacent scars varies from 0.7 duced by protodonatan dragonflies and related paleodictyopteroid to 1.4 mm. All scars have an ovoidal shape and rounded ends, lineages (Labandeira, 2006).

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FIGURE 5—Fossil and extant specimens of Paleoovoidus arcuatum isp. nov: 1, specimen MPEF-IC-1390 a-d (lettered lines) in an indeterminate dicot leaf (RP3, morphotype indeterminate, MPEF-Pb-1612) with a consecutive and parallel pattern of rows, scale bar: 0. 5 cm; 2, extant oviposition of Acantagrion oblutum (Coenagrionidae) on Cynoglossum amabile (Boraginaceae) showing a zigzag pattern and probably the immature aperture observed as a dark lineal in the centre of the scar; 3, two individual eggs and associated callus tissue of Acantagrion oblutum, scale bar: 0.5 cm; 4, specimens MPEF-IC 1393b-d (lettered lines) on an indeterminate dicot (RP3, morphotype indeterminate, MPEF-Pb-2407); scale bar: 0.5 cm; 5, specimens MPEF-IC-1368a-e (lettered lines) showing a distinct zigzag pattern on ‘‘Myrcia’’ deltoidea (LH4, Myrtaceae, MPEF-Pb-1052), scale bar: 0.5 cm; 6, specimen MPEF-IC-1389d, a scar with a circular breached area probably representing the emergence portion of the naiad (arrow) on Lomatia occidentalis (LH2, morphotype TY44, MPEF-Pb-988), scale bar: 1 mm. 438 JOURNAL OF PALEONTOLOGY, V. 83, NO. 3, 2009

PALEOOVOIDUS BIFURCATUS new ichnospecies Occurrence.⎯From the early Eocene Tufolitas Laguna del Figure 2.1, 2.2 Hunco, Chubut Province, Argentina, locality LH13. Discussion.⎯This ichnospecies is comparable with Paleoovo- ‘‘Galle Aceria nervesqua fagina’’ STRAUS, 1977, p. 74, fig. 2, p. idus rectus, as in both cases scars are located in relation to the 78, fig. 50. primary veins. However, in P. rectus there is a single row of scars, ‘‘Lestiden-Typ’’ HELLMUND AND HELLMUND, 1991, p. 4, figs. 1, their long axes approximately parallel with the long axis of the 2; HELLMUND AND HELLMUND, 1996c, p. 160, fig. 16; HELL- leaf and consequently with the midrib or other major vein. The MUND AND HELLMUND, 2002b, p. 49, figs. 1, 2. combination of scar structure and position on the leaf separates ‘‘Oviposition damage on secondary veins’’ LABANDEIRA,WILF, P. bifurcatus from P. rectus and P. arcuatum. This distinctive JOHNSON, AND MARSH, 2007, p. 10. ovipositional pattern corresponds to the damage type DT102 of Diagnosis.⎯Elongate to lens-shaped scars arranged in pairs Labandeira et al. (2007). Patterns similar to P. bifurcatus de- along both sides of a primary vein, forming double rows and scribed here occur throughout the Cenozoic (Hellmund and Hell- sometimes a V-shaped configuration, with the arms of the V par- mund, 1991, 1996c, 2002b); this damage has a sporadic presence allel to secondary veins and the vertex embedded in the midvein. on Mesozoic gymnospermous vegetation (Labandeira, pers. ob- Oviposition scars may continue as a single row of scars located servation.), but is common on Glossopteris leaves from certain in an acute angle along and parallel to one side of the vein. A Late Permian floras of South Africa (Prevec et al., 2009). Pres- dark spot at one extremity of an individual scar very frequently ervation of P. bifurcatus is variable across a broad range of com- touches the primary vein. pression/impression floras, but all occurrences have the signature Description.⎯The holotype occurs in a leaflet of ‘‘Schmidelia’’ ovoidal, ellipsoidal, or teardrop-shaped oviposition scars oriented proedulis, MPEF-Pb-1607. This specimen shows an upper pair of along or within the secondary venation and can occur at variable scars arranged symmetrically about the midvein and parallel to distance from the midrib. secondary veins characterized by a V-shaped configuration along the primary vein. Another pair of scars occurs with a similar V PALEOOVOIDUS ARCUATUM (Krassilov, 2008) configuration, but their arrangement is less clear than for the up- Figures 3, 4, 5.1, 5.4–5.6, 6, 7 per pair. Two additional isolated scars occur at one side of the ‘‘Coenagrioniden-Typ’’ HELLMUND AND HELLMUND, 1991, p. 7, vein in a more basal position with respect to the preceding two fig. 3; HELLMUND AND HELLMUND, 1993, p. 349, fig. 1, p. 350, pairs. The axial length of the scars ranges from 1.7 mm to 2.6 fig. 2; HELLMUND AND HELLMUND, 1996a, p.109, fig. 1a, b; mm, and their width ranges from 0.5 mm to 0.7 mm. The pres- HELLMUND AND HELLMUND, 2002a, p. 255, fig. 1a. ervation of the specimen is poor, and individual scars are only ‘‘Tra¨ufelspitze’’ HELLMUND AND HELLMUND, 1991, p. 291, pl. 1, partially preserved. The first scar occurs at the upper left side of fig. 2. the lamina and is the best preserved; it has a length of 2.6 mm ‘‘Coenagrioniden-Typ vom Bogenmodus’’ HELLMUND AND that may indicate that the remaining scars were probably longer HELLMUND, 1998, p. 282, fig. 1. than the values measured. The minimum distance between the ‘‘Concentric oviposition tracks’’ LABANDEIRA, 2002a, p. 41. scars of the first pair is 0.8 mm and for the second pair is 1.3 ‘‘Radially oriented oviposition scars’’ LABANDEIRA,JOHNSON, mm. The longitudinal distance between two adjacent pairs ranges AND LANG, 2002, p. 312, fig. 8o. from 5.5 mm to 10.7 mm. The greatest distance occurs between ‘‘Ovoposiciones de la Familia Coenagrionidae’’ PEN˜ ALVER AND the second pair of scars and the first scar of the single row. DELCLO` S, 2004, p. 74, fig. 2. The scars often occur in pairs or are isolated and oriented at ‘‘Zygopteran egg sets’’ KRASSILOV,SILANTIEVA,HELLMUND, an acute angle with respect to the vein; their prominence is at- AND HELLMUD, 2007, p. 806, fig. 3a, b, c. tributable to the thickened scar tissue surrounding and probably ‘‘Endophytic oviposition probably of Calopterygina’’ VASILENKO elicited by the inclined, secondary veins. Paired scars do not occur AND RASNITSYN, 2007, p. 1156, figs. 4–6. at the same level on each side of opposite veins, or at the same Sertoveon arcuatum KRASSILOV, 2008, p. 69, fig. 5. transverse position in the case of alternate veined leaves. MPEF- Paleoovoidus arcuatus,VASILENKO, 2008 (new syn.), p. 516, fig. IC 1385 (Fig. 2.2) is an example in which the upper pair of scars 2c, pl. 7, figs. 2, 3. is characterized by the left scar being slightly nearer the tip of Emended diagnosis.⎯Elongate, lens-shaped to teardrop-shaped the leaf than the right one; by contrast, the lower pair shows the scars arranged with the short axes aligned horizontally to each opposite arrangement. other, either as straight rows or as arcs. Frequently the long axes The specimens described by Hellmund and Hellmund (1991, of scars are subparallel to each other. Occasionally, successive 2002b) on Cinnamomum sp. (‘‘Daphnogene’’; Rott locality, Ger- rows are parallel or exhibit zigzag patterns. many, late Oligocene) and on a fragment of an unidentified leaf Description.⎯The shape of the scars ranges from elongate (Geiseltal locality, Germany, middle Eocene) show a scarring ar- (Fig. 5.5), lens-shaped (Figs. 4.1, 4.2, 5.1, 6.5), to teardrop-shaped rangement similar to that described above. In both examples, dou- (Figs. 4.1, 4.3, 4.4, 5.4). The specimens are from 0.9 to 1.6 mm ble rows and single rows were found; in several instances, these in length but only two specimens represent the highest values patterns appeared on the same leaf. In all cases for which a single (Fig. 3.5); widths range from 0.4 to 0.6 mm. The scars in the row was present, there was the continuation of a double row. rows are variously oriented within the leaves, with the long axis However, the double rows show some differences from the Pa- parallel to subparallel to the primary vein (Figs. 3.4, 5.1, 5.4– tagonian specimen. These European specimens were composed of 5.6), perpendicular to it (Figs. 3.1, 3.3), at a highly inclined angle 12 to 16 scars that are separated for short longitudinal distances (Fig. 3.3), or at other inclinations (Fig. 6.1–6.3). The distance between 0.1 to 1 mm, some of which are oriented 90Њ with respect between each scar within a row often is a relatively constant value to the vein. Moreover, the average length, 1.20 mm, is shorter of 1 mm, but in some cases (e.g., Figs. 3.5, 4.1) the scars are than that of the LH specimen. variably separated, with values that range from 0.4 to 2 mm (Fig. Etymology.⎯From the Latin noun, bifurcatus, the condition of 6.3–6.5). Some leaves present distinct and well-defined arcuate having two prongs or forks; masculine. rows from three to 13 scars (Figs. 3.1, 3.2, 4.1, 5.1, 5.6, 6.1–6.3, Types.⎯Holotype specimen MPEF-IC-1385 on the leaflet spec- and 7.2–7.5), in which the acute end of the scar always is ori- imen of ‘‘Schmidelia’’ proedulis (Sapindaceae) MPEF-Pb-1607 entated in the same direction (Figs. 3.1, 4.4, 5.4). In other cases (Fig. 2.1, 2.2). the arcuate rows are parallel to each other and are arranged en Examined material.⎯The same as the holotype. echelon (Figs. 3.4, 3.5, 4.1, 5.1, 5.5, 6.2), with scars of each SARZETTI ET AL.—EOCENE ODONATAN OVIPOSITION FROM PATAGONIA 439

FIGURE 6—Specimen of Paleoovoidus arcuatum on the holotype of ‘‘Anona’’ infestans from Rı´o Pichileufu´ (Berry, 1938) (morphotype unknown, type material, USNM 40389a,b): 1, entire leaf fossil showing the distributions of scars over the lamina, scale: 1 cm; 2, specimens USNM 40389a-b (lettered lines) 6.3–6.5, details of individual scars, scales: 1 cm (Fig. 6.1, 6.2), 1 mm (Fig. 6.3, 6.4), and 0.1 mm (Fig. 6.5). 440 JOURNAL OF PALEONTOLOGY, V. 83, NO. 3, 2009

FIGURE 7—Additional specimens of Paleoovoidus arcuatum isp. nov. exhibiting an overlapping distribution of oviposition scars (Fig. 7.1, 7.2, 7.4) and clearly demarcated rows (Fig. 7.3, 7.5): 1, MPEF-IC-1367 in an unknown dicot leaf (LH4, morphotype TY122, MPEF-Pb-1051) [note continuous linear file of oviposition marks at bottom of leaf (arrow)], scale bar: 1 cm; 2, MPEF-IC-1391 in an unknown dicot leaf (RP2, morphotype indeterminate, MPEF-Pb- 1613); 3, MPEF-IC-1375 in an unknown dicot leaf (LH2, morphotype indeterminate, MPEF-Pb-1588), scale bar: 1 cm; 4, enlargement from rectangular template in Figure. 7.1, showing detail of oviposition scars exhibiting dark spots (arrows) at the narrow end of each ovoidal scar; 5, MPEF-IC-1377 on ‘‘Cassia’’ argentinensis (LH4, morphotype TY117, MPEF-Pb-1589); scale bar: 0.5 cm. consecutive row arranged regularly with minimal deviation of leaf tissue between two adjacent scars is broken or removed (Fig. scars within a row. These rows may be subparallel to each other 5.5). In other specimens (Figs. 3.2, 4.3, 4.4, 5.6, 6.4), the blunt (Figs. 4.1, 6.2) or convergent in one or more points that result end of the scars displays a rounded hole, indicating the absence from projected lines drawn perpendicular to the multiply oriented of plant tissue, resulting in a whitish area. In these same speci- oviposition rows (Fig. 3.4) (Hellmund and Hellmund, 1991, fig. mens, and in others (Figs. 5.6, 6.4), a dark spot at one end is 6). In other cases (Figs. 3.1, 5.5) the arcuate rows are not parallel observed, which is most clearly distinguished at the acute ends to each other, the terminus of one approaching the terminus of of teardrop-shaped scars (Figs. 3.5, 4.1). the next one, resulting in a zigzag pattern. In some specimens the Chaotic ovipositional patterns on leaves as in Figure. 7.1 may SARZETTI ET AL.—EOCENE ODONATAN OVIPOSITION FROM PATAGONIA 441 result in uninterpretable behavior. However, closer examination The diagnosis is emended herein to include scars of a broader reveals that rows of distinctive oviposition scars have been over- range of shape (elongate, lens-shaped and teardrop-shaped) that printed (Fig. 7.1, 7.4), with individual scars having an elongate- are distributed both in linear rows and in arcs, which in some to lens-shaped structure with an enveloping raised rim and a cen- cases can exhibit a zigzag trajectory. Oviposition specimens that tral depression, often housing a dark circular region at one an- exhibited a zigzag pattern were referred by Krassilov and Silan- gulated end (Fig. 7.4). There is discernable alignment of scars tieva (2008) to a similar ichnospecies, Catenoveon undulatum. into particular rows and arcs. Targeted host plants typically are Nevertheless, the principal difference between C. undulatum and robustly constructed pinnate leaves with prominent midveins. P. arcuatum is the relationship with the primary vein, which is Material examined.⎯Specimen MPEF-IC 1367, on an unaffil- absent in the later. Moreover, P. undulatum is the only ichno- iated dicot (LH4-1213, morphotype TY122 of Wilf et al., 2005a), species with scars distributed in the leaf lamina without any ap- specimen MPEF-IC-1368a–e, on ‘‘Myrcia’’ deltoides, (LH4, Myr- parent relation to the primary vein, a feature that differentiates it taceae, MPEF-Pb-1052); specimen MPEF-IC-1369, on ‘‘Myrcia’’ from P. bifurcatus scars that are inclined to the primary vein and chubutensis, (LH13, Myrtaceae, MPEF-Pb-2217); specimen from P. rectus scars that occur along major veins. Several authors MPEF-IC-1370a–f, on ‘‘Celtis’’ ameghenoi (LH2, MPEF-Pb- have documented scars exhibiting patterns similar to the material 1053); specimen MPEF-IC-1371a–c, on an unaffiliated dicot described here under P. arcuatum. Hellmund and Hellmund (LH6, MPEF-Pb-1054, morphotype indeterminate); specimen (1991, 1993, 1996c, 1998, 2002a), in particular have described MPEF-IC-1372a–e, on an unaffiliated dicot (LH2, MPEF-Pb- and figured numerous specimens with identifiable scar patterns, 1584); specimen MPEF-IC-1373a–f, on ‘‘Myrcia’’ chubutensis including examples from Kounice and Vysˇehorˇovice (both Upper (LH13, Myrtaceae, MPEF-Pb-2215); specimen MPEF-IC- Cretaceous) in Bohemia, Czech Republic; and from Messel (mid- 1374a–c, on ‘‘Cupania latifolioides’’ (LH18, ?Cunoniaceae, dle Eocene), Salzhausen (middle Miocene), Rott (upper Oligo- MPEF-Pb-1585); specimen MPEF-IC-1375, in an unaffiliated di- cene), Hammerunterwiesenthal (upper Oligocene), and Berzdorf cot (LH2, morphotype indeterminate, MPEF-Pb-1588); specimen and Randecker Maar (both lower Miocene) in Germany. They MPEF-IC-1377, on ‘‘Cassia’’ argentinensis (LH4, morphotype distinguished between smaller scars, 1.3 to 1.4 mm in length, TY117, MPEF-Pb-1589); specimen MPEF-IC-1378a–e, on Lo- present as an arcuate, parallel pattern, versus larger scars, 1.6 to matia occidentalis, (LH4, Proteaceae, MPEF-Pb-998); specimen 1.8 mm long, deployed in a zigzag pattern. The material docu- MPEF-IC 1380a–c, on an unaffiliated dicot leaf (LH13, MPEF- mented by Pen˜alver and Delclo`s (2004) from the ‘‘La Rincon˜ada’’ Pb 1591); specimen MPEF-IC-1381, on Malvaceae (LH6, mor- site at the Ribesalbes locality (early Eocene, in Castello´n, Spain) photype TY23, MPEF-Pb-1592); specimen MPEF-IC-1383, on an also show parallel rows occurring in a zigzag pattern from dif- unaffiliated dicot (LH4, morphotype TY170 of Wilf et al., 2005a, ferent species composed of ovoidal-oblong scars, with values that MPEF-Pb-1605); specimen MPEF-IC-1384a,b, on an unaffiliated range from 0.9 to 1.1 mm in length and from 0.2 to 0.3 mm in dicot (LH17, morphotype indeterminate, MPEF-Pb-1606); speci- width. Moreover, the traces documented by Labandeira (2002a), men MPEF-IC-1386a–c, on an unaffiliated dicot (RP3, morpho- from the middle Eocene Republic Flora of eastern Washington, type indeterminate, MPEF-Pb-1608); specimen MPEF-IC- USA, show similar patterns that were defined as separated, equal- 1388a–f, on an unaffiliated dicot (RP3, morphotype sized, lenticular scars, arranged in semicircular arcs. Scars from indeterminate, MPEF-Pb-1611); specimen MPEF-IC-1389a–f, on the latest Cretaceous Hell Creek Formation of North Dakota, Lomatia occidentalis (LH2, Proteaceae, MPEF-Pb-988); specimen USA, show similar morphologies to the ones described here but MPEF-IC-1390a–f, on an unaffiliated dicot (RP3, morphotype in- lack a clear pattern of arrangement (Labandeira et al., 2002). Re- determinate, MPEF-Pb-1612); specimen MPEF-IC-1391, on an cently, Vasilenko (2007, 2008) described specimens on the float- unaffiliated dicot (RP2, morphotype indeterminate, MPEF-Pb- ing leaves of Quereuxia possessing elongate oviposition scars of 1613); specimen MPEF-IC-1392, on ‘‘Myrcia’’ chubutensis 0.75 to 0. 85 mm in length and 0.13 mm in width, distributed in (LH13, morphotype TY21, MPEF-Pb-2406; specimen MPEF-IC- parallel rows. The Quereuxia material is from the Maastrichtian 1393a–e, on an unaffiliated dicot (RP3, morphotype indetermi- age and originates from the Udurchukan locality of the Amur nate, MPEF-Pb-2407); and specimen USNM 40389a,b on the ho- Region, Russia. lotype of ‘‘Anona’’ infestans (type material). Berry (1938) described scars on the holotype of ‘‘Anona’’ in- Occurrences.⎯From the early Eocene Tufolitas Laguna del festans from the Rı´o Pichileufu´ paleoflora that clearly represent Hunco Formation, Chubut Province, and from the middle Eocene P. arcuatum ovipositional damage (Fig. 6.1–6.5). However, he Rı´o Pichileufu´ locality, Rı´o Negro Province, Argentina. suggested that these marks could represent the bodies of scale Discussion.⎯In his recent contribution, Vasilenko (2008) in- insects (Hemiptera: Coccoidea). This leaf (Fig. 6) shows many cluded in the ichnogenus Paleoovoidus two new ichnospecies, P. arcuate rows, either parallel or in a zigzag pattern, of lenticular flavellatus and P. arcuatus. The former ichnospecies was de- to teardrop scars distributed over most of the lamina. The tem- scribed as ‘‘arched oviposition distributed in rows and separated poral occurrence of distinctive Paleoovoidus arcuatum, unlike P. by distance about a maximum width of the eggs or somewhat rectus, and P. bifurcatus, probably is confined to the Cenozoic larger.’’ This differs from P. arcuatus in having shorter distances and Late Cretaceous; no known occurrences antedate the appear- between scars. By contrast, P. arcuatus has slightly arched ovi- ance of angiosperms during the mid Early Cretaceous. position scars, with the eggs set in rows at considerable distance from each other parallel to their long axes. This ichnospecies is DISCUSSION more similar to the patterns observed in the Patagonian leaves. Endophytic oviposition has considerable potential for the study However, a few months prior to Vasilenko’s paper, Krassilov of dragonfly host-plant use and behavioral evolution. This is at- (2008) established a similar ichnogenus named Sertoveon which tributable to the fact that the insertion of the ovipositor into plant he described as ‘‘egg scars in transverse rows or arches, inserted tissue results in a persistent, fossilizable scar of callus tissue that at about right angles to the direction of the row.’’ Likewise, he surrounds inserted, typically nonpreserved eggs. This distinctive, erected two new ichnospecies, S. cribellum and S. arcuatum. convex, ovoidal damage has an extensive fossil record on various These two ichnospecies also resemble closely the pattern de- plant tissues, displaying a characteristic pattern of linear, curvi- scribed in our material. We consider that both ichnospecies, P. linear or arcuate rows that occur in plant organs as dark, oval, to arcuatus and S. arcuatum, represent the same oviposition pattern. teardrop-shaped scars (Labandeira, 2002a, 2006). In many cases, However, according to the ISCN rules, Paleoovoidus has nomen- ovipositional patterns occur in a parallel or zigzag fashion, or clatorial priority and is the valid ichnogenus; P. arcuatum is the alternatively, in no pattern at all. By contrast, in exophytic ovi- correct ichnospecies. position, eggs often are distributed in tight packets or as looser 442 JOURNAL OF PALEONTOLOGY, V. 83, NO. 3, 2009 clusters on the leaf surface (Corbet, 1999; Labandeira, 2002a; 1996b, 1996c, 1998, 2002a), and typically involve damselfly ovi- Labandeira et al., 2007; Vasilenko and Rasnitsyn, 2007; Krassilov position. The German mid-Cenozoic occurrences reveal consid- and Silantieva, 2008; Vasilenko, 2008). Moreover, exophytic ovi- erable behavioral information and are directly comparable with position is done by insects either lacking an external ovipositor extant oviposition patterns and associated behaviors. or possessing a modified, nonslicing ovipositor (Labandeira, The biology and paleobiology of odonatan oviposi- 2006), and any resulting effects on plant surface features rarely tion.⎯Odonatan oviposition patterns have received considerable preserve as fossils. In addition, egg morphology also can be useful attention in ecological studies, particularly those emphasizing en- to distinguish the type of oviposition, when infrequently present dophytic placement and behavior (Wesenberg-Lund, 1913a, (e.g., Sahle´n, 1995; Vasilenko and Rasnitsyn, 2007; Vasilenko, 1913b, 1943; Schiemenz, 1957; Jurzitza, 1974; Grunert, 1995; 2008; Pott et al., 2008; Krassilov and Silantieva, 2008). Corbet Hellmund and Hellmund, 1998; Corbet, 1999). Matushkina and (1999) characterized endophytic odonatan eggs as rather elongate, Gorb (2007) have emphasized that females of most odonate spe- often flattened, and several times longer than wide, whereas exo- cies deposit their eggs into a plant substrate. Females use the two phytic eggs are more ellipsoidal to subspherical. sets of valves of the ovipositor to penetrate and cut leaf tissue, Fossil record of insect oviposition.⎯Ichnofossils of oviposi- inserting eggs within surface or deep tissue (Matushkina and tional traces have been recognized principally in sphenopsid stems Gorb, 2007; Corbet, 1999; Miller and Miller, 1988; Labandeira, and seed-plant leaves (Roselt, 1954; Kelber, 1988; Schaarschmidt, 2006). Typically, one egg is deposited for each insertion (Tillyard, 1992; Johnston, 1993; Grauvogel-Stamm and Kelber, 1996; Zher- 1917; Ando, 1962; Hellmund and Hellmund, 2002a; Sahle´n, ikhin, 2002; Banerji, 2004; Beattie, 2007). The oldest record of 1995; Lutz and Pittman, 1968). oviposition is from an arborescent Pennsylvanian age sphenopsid, The Anisoptera (dragonflies) display a wide variety of ovipo- Calamites cistii, bearing pronounced, ellipsoidal scars that were sitional modes, involving both exophytic and endophytic egg attributed to the Archaeorthoptera or Palaeodictyoptera (Be´thoux placement (Corbet, 1999). However, patterns of endophytic plant et al., 2004). The oldest trace fossils assigned to odonatan ovi- damage are poorly described in the literature for this group, and position, referred to the Protodonata, comes from the Lower the behaviors and mechanisms of egg insertion within leaves or Permian flora of the Rı´o Bonito Formation, Brazil (Adami-Ro- other plant organs are largely unknown. Considerably more is drigues et al., 2004). Later Paleozoic endophytic oviposition, such known of extant zygopteran ovipositional behavior, in which scars as that from the Upper Permian of Australia, is recognizable but typically are narrow and have an oval to ellipsoidal surface ex- difficult to assign to a particular producer. For example, an upper pression. For example, the eggs of Lestes eurinus were described Permian flora from southeastern Australia reveals small circular by Lutz and Pittman (1968) as elongate, cylindrical, and uniform insertion scars grouped into several clusters in the foliage of the in size. Modern field and laboratory observations at Horco Molle, extinct sphenopsid cladode Phyllotheca (Beatty, 2007). Presum- in Tucuma´n Province, Argentina, were made for oviposition of ably, these scars were induced by a member of the Protodonata Acanthagrion ablutum (Zygoptera: Coenagrionidae) (Calvert, or Palaeodictyopteroidea, paleopterous clades that largely became 1909) on Cynoglossum amabile (Boraginaceae) leaves and for extinct at the end Permian (Labandeira, 2006). oviposition of the same zygopteran species on Polygonum punc- Pre-Cretaceous, Mesozoic evidence for odonatan ovipositional tatum (Polygonaceae) at Dique Escaba, in southern area of Tu- damage predominantly originates from biogeographically dispa- cuma´n Province. Both of these modern examples display eggs rate Middle and Upper Triassic sites worldwide, and from the with a general ellipsoidal shape, whose ends are acute, rounded, European Lower Jurassic. The most important odonatan ovipo- or blunt in shape. The egg structure is characterized by a yellow- sition occurrences, unaffiliated to family, are from the Middle and ish to brownish region, which in a few cases bears a small, linear Upper Triassic of France and Germany (Grauvogel-Stamm and aperture (Fig. 5.2, 5.3). However, in some cases a white aperture Kelber, 1996). In particular, Pott and colleagues (2008) docu- at one end also is observed. This last pattern matches the ovi- mented spectacular material, replete with microstructural details positional scars in the fossils (Fig. 5.6). of insect egg and adjacent plant cuticle, from the Upper Triassic Fossil ovipositional scars described herein and in the literature of Austria. Gondwanan occurrences from the Upper Triassic of share with extant odonatan egg insertions a similar general shape. Chile (Gnaedinger et al., 2007) and especially the Molteno For- mation of South Africa (Labandeira, 2006), have documented sev- This similarity ranges from scars with two similar extreme, round- eral distinctive ovipositional types (Labandeira et al., 2007). Van ed, or more tapering points, but in other cases with a blunt and Konijnenburg-van Cittert and Schemießner (1999) have docu- acute end resulting in a teardrop shape. Hellmund and Hellmund mented younger, new types of ovipositional damage from the (2002a) noted that several scars possess raised encircling rims and Lower Jurassic of Bavaria (Germany) that may represent an ex- have a smooth concavity in the central area. They also argued pansion of dragonfly egg-laying strategies from the earlier Tri- that small protrusions in the interior depression of the scars could assic. be the remnants of egg envelopes. These features were not ob- More recent, better-defined, endophytic oviposition damage, at- served on our material. In some specimens (Figs. 3.3, 5.5), a tributable to particular modern lineages, becomes abundant during visible dark spot was observed at the angulate scar end. The same the Cretaceous and especially the Cenozoic (Hellmund and Hell- feature was observed by Krassilov et al. (2007) but described as mund, 1991, 1993, 1996a, 1996b, 1996c, 1998, 2002a; Lewis, preserved callus tissue. By contrast, Krassilov and Silantieva 1992; Labandeira, 2002a, 2002b; Labandeira et al., 2002; Pen˜al- (2008) show a slender dark band inside the egg impression that ver and Declo`s, 2004; Vasilenko, 2005, 2008; Vasilenko and Ras- was interpreted as a dried yolk sac or an exuvium of an embryonic nitsyn, 2007; Krassilov et al., 2007; Krassilov and Silantieva, larva. 2008). As in Triassic and Jurassic examples of oviposition, Cre- In other cases (Figs. 4, 5.2, 5.6), scars display a blunt end taceous and Cenozoic material is attributed commonly to the cradling a more centrally positioned, rounded or more linear hole Odonata, or occasionally to other groups such as the Diptera, that is distinguishable as a clear zone because of the absence of Lepidoptera, Coleoptera, Hymenoptera and Hemiptera (Krassilov plant tissue. This distinctive zone, observed both in the fossils and Silantieva, 2008). Specimens referred originally as coleop- and in one leaf from the Dique Escaba locality, may represent an terous eggs in Alnus (Betulaceae) leaves (Lewis and Carroll, emergence aperture, indicating that the immature nymph had 1991, 1992; Lewis, 1992), later were reidentified as odonatan ovi- abandoned the foliar microenvironment for life in water (Fig. 5.6). positional damage (Labandeira, 2002a). Many of these docu- Ovipositional behavior varies among the major groups of mented descriptions come from the Cenozoic of Germany and Odonata, resulting in a diversity of patterns that characterize ex- were evaluated by Hellmund and Hellmund (1991, 1993, 1996a, tant and fossil damage on leaf surfaces. Observations of extant SARZETTI ET AL.—EOCENE ODONATAN OVIPOSITION FROM PATAGONIA 443

Zygoptera show that there are differences in ovipositional behav- The same pattern has been observed by Hellmund and Hellmund ior, for example between Coenagrionidae and Lestidae (Gower (1991, 1996a) in various dicot leaves. Some specimens (Fig. 2.2, and Kormondy, 1963; Lutz and Pittman, 1968; Hellmund, 1991, 2.3) display subparallel ovipositional insertion in a single row, of 2002b; Matushkina and Gorb, 2007). The endophytic oviposition which individual scars may occur in both midrib vascular tissue of Coenagrionidae includes more-or-less a 1 mm spaced distance and in the leaf-blade. This pattern also consists of scars that ap- between the oviposition scars that form linear rows, which are pear in a single, straight row described by Vasilenko (2005) and either slightly crescentic, semicircular, or parallel, or alternatively herein, but it has not been documented extensively in modern deployed as a zigzag pattern (Wesenburg-Lung, 1913a, 1913b; foliar material. Grunert, 1995; Hellmund and Hellmund, 1991, 1998). Paleoo- Some of our specimens (Fig. 7.1–7.5), included under Paleoo- voidus arcuatum clearly resembles this range of pattern. Hell- voidus arcuatum, show some disorder in the distribution of scars mund and Hellmund (1991) were the first to attribute similar pat- in contrast to the distinctive patterns described previously. This terns in fossil leaves to ovipositional traces of Odonata from the more chaotic distribution may be related to the high density of upper Oligocene of Rott, Germany. These authors originally scars, which would preclude identification of individual rows, named the arcuate and parallel rows as Bogenmodus, and the zig- possibly because of superimposed, multiple ovipositional events zag rows as Zickzackmodus. These alternative styles were com- by one or several females in the same leaf. Alternatively, elevated pared to extant ovipositional damage in leaves made by damsel- scar density may be attributable to the normal reproductive be- flies, particularly the Coenagrionidae, and this clade was havior of an unknown, ovipositing odonatan. This latter alterna- determined to be the producer of this pattern. Later, new fossil tive is less likely because distinct linear files of scars were de- evidence from the Hell Creek Formation (Upper Cretaceous) of tectable and apparently were overprinted with subsequent waves North Dakota, U.S.A., attributed oviposition damage on leaves of of oviposition. Marmarthia pearsonii (Laurales) and Erlingdorfia montana (Pla- Analyses of the distribution of oviposition scars on fossil leaves tanaceae) to the Coenagrionidae (Labandeira et al., 2002). More- and their comparison to patterns obtained from extant autecolog- over, Pen˜alver and Delclo`s (2004) documented Miocene ovipo- ical studies is important for the interpretation of these ichnofos- sition trace fossils of Coenagrionidae from La Rincon˜ada, Spain, sils. This allows for an understanding of the ovipositional behav- on leaves of Laurophyllum (Lauraceae), Caesalpinia (Fabaceae), ior that produced the original damage. Especially in Paleoovoidus and Populus (Salicaceae). Similar ovipositional patterns from the arcuatum, the orientation of each scar in an arcuate or zigzag Eocene of Washington were observed by Labandeira (2002a) for trajectory can indicate the position of the female on the leaf dur- Betula (Betulaceae), Crataegus, Paracrataegus, Sorbus (all Ro- ing oviposition (Hellmund and Hellmund, 1991). Accordingly, if saceae), and Ginkgo (Ginkgoaceae), some of which initially and lines are drawn perpendicular to each linear file of scars, the point incorrectly were attributed to beetles (Chrysomelidae) by Lewis where these lines converge, through triangulation, should be the and Carroll (1991, 1992). Likewise, Vasilenko and Rasnitsyn abdominal pivot point represented by an anchored thorax. When (2007) and Vasilenko (2008) described several examples of elon- the scars are teardrop-shaped, the abdominal pivot point is more gate and oval endophytic oviposition on leaves of Quereuxia that precisely identifiable because the shape of eggs allows a sharper were assigned to the ichnotaxonomic group, Paleoovoididae, from definition of the perpendicular lines. From this pivot point, the the Maastrichtian of the Udurchukan locality in the Amur Region female lays eggs by swinging her abdomen from one side to the of Russia. other, depositing from three to fifteen eggs during each swipe. Body fossils of Coenagrionidae are known from several Early The next row likewise is produced after she moves a single step Cretaceous localities (Jarzembowski, 1990; Jarzembowski et al., forward and inscribes another swinging movement of her abdo- 1998; Jell, 2004). It is unclear if Paleoovoidus arcuatum origi- men (Hellmund and Hellmund, 1991; Pen˜alver and Delclo`s, nated within the Coenagrionidae or possibly from an earlier Me- 2004). The abdominal pivot point potentially is moved along the sozoic ancestor shared with the sister-clade Platycnemidae (Be- same axis when producing different arcs of scars, resulting in a chley, 1996), which generates a similar pattern of oviposition distinctive and successive series of en echelon files (Hellmund (Watanabe and Atachi, 1987). A similar pattern of damage, found and Hellmund, 2002a). These parallel and zigzag patterns may be in Agrion (Wesenberg-Lund, 1943, fig. 57), a member of the dis- tant zygopteran clade Calopterygidae, may represent behavioral combined in the same ovipositional behavior, as shown by field convergence. observations at Horco Molle and Escaba in northwestern Argen- A different mode of oviposition is represented by species of tina. Oviposition begins with well-defined and independent Lestidae that lay eggs in double rows at both sides of a primary curved rows, continues with increasingly arcuate files, and results vein or occasionally in a single row along one side of the vein. finally in a zigzag configuration. This observation indicates that At insertion, lestid eggs normally are oriented from an acute to a the same female can produce both types of patterns, Bogenmodus perpendicular angle relative to a major vein. Structural details of and Zickzackmodus, from the same ovipositional pivot point, the ovipositional process were provided by Matushkina and Gorb which should discourage the possibility of separating ichnospecies (2007), including the ovipositional behavior of Lestes sponsa and based on this modern behavioral character. L. barbarus, indicating that the major axis of paired or single Other behavioral traits are reflected in the ichnospecies de- eggs is parallel to plant fibers. Similarly, the fossil oviposition scribed herein. Some members of the Lestidae insert their eggs pattern described here and assigned to Paleoovoidus bifurcatus on plant stems near water, instead of leaves. Hellmund and Hell- probably was produced by damselflies of the family Lestidae. mund (1991) mentioned that Lestidae lay eggs at the sides of a Hellmund and Hellmund (1991, 1996c, 2002b) described the primary leaf vein, usually a midrib, and inferred that they used same type of oviposition that we attribute to P. bifurcatus in a this anatomic structure as a guide. (The use of a prominent vein leaf of Cinnamomum sp. (‘‘Daphnogene,’’ Lauraceae) from the as a guide may have an evolutionary relationship with linear ovi- late Oligocene and in a unidentified leaf from the middle Eocene position on stems, extending to the late Paleozoic.) The eggs are of Germany, a pattern they named Doppelreihenmodus. inserted into foliar tissue by moving the abdomen once to the Ovipositional damage distributed in a single row, assigned here right and then to the left for each oviposition point, producing to Paleoovoidus rectus, also has been attributed to the Lestidae often paired files along the vein (Hellmund, 1991, 2002a). Ob- based on extant foliar damage patterns. Modern lestid oviposi- servations made on the reproductive habits of extant Lestes rec- tional scars have been observed to occur within major veins form- tangularis Say 1839 on leaves of Rumex (Polygonaceae), Typha ing a single concatenated row, characterized by parallel alignment (Typhaceae) and Scirpus (Cyperaceae), from Pennsylvania, of long axes of the elongate scars (Gower and Kormondy, 1963). U.S.A., showed that females rotate the last eight to ten abdominal 444 JOURNAL OF PALEONTOLOGY, V. 83, NO. 3, 2009 segments 90 degrees to produce this pattern (Gower and Kor- likely to be Lestidae and Coenagrionidae. Based on these Pata- mondy, 1963). By contrast, coenagrionid oviposition appears not gonian occurrences and evidence for distinctive damselfly ovi- to be influenced by vein architecture during selection of the foliar positional damage, we infer that, by the early to middle Eocene area for egg insertion. This type of oviposition targets different boundary interval, species of the Lestidae and Coenagrionidae regions of the leaf without restriction and produces canted ori- and their ovipositional behaviors probably were present at the LH entations of scar files. and RP localities. Host-plant preferences.⎯Observations regarding host-plant preferences for endophytic oviposition have been made for sev- CONCLUSIONS eral extant zygopteran species (Gower and Kormondy, 1963; Bick 1. Evidence of endophytic odonatan oviposition is documented and Hornuff, 1965). Corbet (1963) showed that some zygopteran from the Laguna del Hunco (LH, early Eocene) and Rı´o Pichi- species chose one type of plant for oviposition among several leufu´ (RP, middle Eocene) floras of Patagonia, Argentina. Three available alternatives. Similar results were obtained by Lutz and types of oviposition are described from LH, assigned to the three Pittman (1968) who concluded that Lestes eurinus Say, 1839 ovi- newly defined ichnospecies Paleoovoidus rectus and Paleoovo- posited only in Sparganium americanus (Sparganiaceae). How- idus bifurcatus, as well as the previously established Paleoovo- ever, Kumar and Prasad (1977) did not note any host-plant pref- idus arcuatum of Krassilov and Silantieva (2008). By contrast, erence in their study of the reproductive behavior of Neurobasis only P. arcuatum is recorded from the RP paleoflora. Ichnospe- chinensis (Calopterygidae), which oviposited endophytically in cies of Paleoovoidus include elongate to lens-shaped or teardrop- several species of riparian plants. shaped scars expressed on the surfaces of foliar tissue that are Only a few of our leaf specimens, each with oviposition scars arranged in distinctively regular or otherwise random patterns. In at LH or RP, represent the ichnospecies Paleoovoidus rectus and some cases, the narrow end of the scar bears a dark spot, but in P. bifurcatus. Given the paucity of occurrences, it is impossible other instances, there is a broader, circular, small depression to determine if ovipositional specialization was present for P. rec- lodged at the wider end. Both of these features suggest apertures tus and P. bifurcatus. By contrast, comparatively abundant Pa- for the emergence of dragonfly (odonatan) immatures. leoovoidus arcuatum is represented by ovipositional damage on 2. By comparison with similarities in morphology with extant a wide variety of foliage, including specimens of Lauraceae, Pro- oviposition patterns, ichnospecies of Paleoovoidus are attributable teaceae, Fabaceae, Malvaceae, Cunoniaceae, and Myrtaceae. Sup- to recognizably modern types, specifically to the Suborder Zyg- porting this broad spectrum of plant hosts, P. arcuatum only oc- optera. Paleoovoidus rectus and P. bifurcatus. probably were pro- curs more than once per species in two specimens each of duced by members of the Family Lestidae; P. arcuatum was pro- ‘‘Myrcia’’ chubutensis and Lomatia occidentalis. These observa- duced by members of the Family Coenagrionidae. tions indicate that no preferential host-plant preference was pres- 3. The same patterns of egg insertion, particularly for the more ent for damselflies in their selection of oviposition leaf substrates. ⎯ abundant Paleoovoidus arcuatum, were present for several leaf The South American odonatan body fossil record. South morphotypes, but no host-plant specificities were observed. America has a significant body-fossil record of Odonatoptera, par- 4. Evidence from the Eocene of South America demonstrate ticularly because the wings of dragonflies and damselflies pre- that certain odonatan taxa have maintained similar patterns and serve well. From the Paleozoic and Mesozoic of Brazil, several behaviors of endophytic oviposition, represented by scars distrib- families are known (Martins-Neto, 2005; Moura et al., 2006), par- uted in linear, zigzag, or otherwise parallel traces over leaf lam- ticularly from the Early Permian of the Parana´ Basin and the Early inae for approximately a 50 million-year interval. These behav- Cretaceous of the Araripe Basin. By contrast, in Argentina odo- iors, by virtue of their ichnotaxonomic synonymy with earlier natopteran body-fossil specimens overwhelmingly originate from Early Jurassic to Late Cretaceous occurrences, considerably an- Cenozoic deposits (Petrulevicˇius, 2001; Petrulevicˇius et al., 1999; tedate the mid Paleogene, and extend deeper into the Mesozoic. Petrulevicˇius and Nel, 2002a, 2002b, 2003a, 2003b, 2004a, 2004b, 2005, 2007). There are a few records from the Paleozoic ACKNOWLEDGMENTS of Argentina, including two members of the Geroptera in the Ear- ly Pennsylvanian (Riek and Kukalova´-Peck, 1984; Wootton et al., We are grateful to Roberto Straneck for his excellent assistance 1998; Gutierrez et al., 2000), and multiple occurrences of the with German translation. We thank Alejandra Molina for her help Odonata from the Middle and Late Triassic (Carpenter, 1960; with field research in collecting extant odonatan oviposition, and Martins-Neto et al., 2003). Additionally, Petrulevicˇius and Nel to Alberto Slami for his help with the plant identifications. For (2003a, 2005, 2007) previously documented body fossils (wings) helpful reviews of the manuscript, we thank J. Petrulevicˇius and of Odonata from the Laguna del Hunco locality. One zygopteran D. Vasilenko. In addition, we acknowledge M. Caffa, L. Canessa, specimen was assigned to the extinct family Austroperilestidae B. Cariglino, I. Escapa, M. Gandolfo, C. Gonza´lez, R. Horwitt, (Austroperilestes hunco) and possibly is related to the extant fam- P. Puerta, E. Ruigomez, H. Smekal, and S. Wing for invaluable ily Perilestidae. The other specimen was assigned to the new ex- assistance in the field and laboratory. This work was supported tinct family Frenguelliidae (Frenguellia patagonica). The Austro- by the Proyecto de Investigacio´n Cientı´fica y Tecnolo´gica (PICT) perilestidae and Frenguelliidae records currently represent the 13286 to J. F. Genise; National Science Foundation Grant DEB- only body-fossil evidence for Odonata from LH; neither family 0345750 to PW, CCL, NRC, and KRJ; National Geographic So- has been documented at RP. These taxa conceivably could have ciety grant 35229-G2 to PW and NRC; the Evolution of Terres- produced any of the ichnotaxa observed on LH leaves, but there trial Ecosystems Consortium of the National Museum of Natural is no evidence for or against this other than the presence of the History to LCS; and the Smithsonian Institution Small Grants body fossils. It bears re-emphasis that neither the Coenagrionidae Fund to CCL. Thanks go to Finnegan Marsh for the final draft of nor Lestidae are known from body fossils at either locality. the figures, and to the Nahueltripay family and INVAP (Instituto Currently the oldest reliable evidence worldwide of Lestidae is de Investigaciones Aplicadas) for land access. This is Contribu- ovipositional traces from the middle Eocene of Germany (Hell- tion 163 of the Evolution of Terrestrial Ecosystems Consortium mund and Hellmund, 2002b). 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