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Late Pleistocene galls from the La Brea Tar Pits and their implications for cynipine wasp and native plant distribution in southern California
YQRES-03676; No. of pages: 10; 4C: Quaternary Research xxx (2015) xxx–xxx
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Late Pleistocene galls from the La Brea Tar Pits and their implications for cynipine wasp and native plant distribution in southern California Anna R. Holden a,b,c,⁎, Diane M. Erwin d, Katherine N. Schick e, Joyce Gross f a
Richard Gilder Graduate School at the American Museum of Natural History, 79th at Central Park West, New York City, NY 10024, USA Department of Entomology, Natural History Museum of Los Angeles County, 900 Exposition Boulevard, Los Angeles, CA 90007, USA La Brea Tar Pits and Museum, 5801 Wilshire Boulevard, Los Angeles, CA 90036, USA d Museum of Paleontology, University of California, Berkeley, CA 94720, USA e Essig Museum of Entomology, University of California, Berkeley, CA 94720, USA f Berkeley Natural History Museums, University of California, Berkeley, CA 94720, USA b c
a r t i c l e Article history: Received 6 May 2015 Available online xxxx Keywords: Paleoenvironment Cynipine Gall Rancho La Brea Pleistocene
i n f o
a b s t r a c t Thirteen intact cynipine galls (Cynipidae) are identified from the significant late Pleistocene locality of Rancho La 14 Brea, mostly within the range of approximately 30,000 to 48,000 C yr BP. Late Cenozoic cynipids have a poor fossil record; it is thus of great interest that the provisional dates for this fossil gall collection establish that these insects and their hosts were an important part of the late Pleistocene ecosystem in and around Rancho La Brea. Cynipine host specificity both verifies, as well as augments, the proportionally low record of plants recovered at Rancho La Brea in comparison to records of mammals, birds, and other fauna. Because galler and hosts represent extant species, their climate and habitat restrictions offer a good basis for making paleoecological inferences. In particular, they imply that many of the diverse habitats found in California today, or, at least plant associations with similar environmental restrictions, some presently a distance from the Rancho La Brea Tar Pits, existed in the vicinity of this locality during the late Pleistocene. This material also includes previously undescribed species, several of which are morphologically similar to extant comparative material that exhibits a “jumping” behavior, previously believed to be unique to Neuroterus saltatorius Edwards. © 2015 University of Washington. Published by Elsevier Inc. All rights reserved.
Introduction The Rancho La Brea Tar Pits, one of the world's richest and most important Ice Age fossil localities, is particularly celebrated for its extinct large mammal fauna, which included species such as sabertooth cats (Smilodon), dire wolves (Canis dirus), and mammoths (Mammuthus). But this locality is also prized for yielding other kinds of fossils, asphaltimpregnated invertebrates, and plants. Such three-dimensional fossils may exhibit structural details that provide a means for securely identifying species that have not been studied as much in depth as the so-called “trophy” fossils from Rancho La Brea (Stock and Harris, 1992). The collection of thirteen galls identified in this study not only show the potential for acquiring novel paleoecological information from still-unstudied insects and plants from this locality but also augments the paltry fossil gall record for all gall inducers and for fossils that should be reported in greater abundance (Larew, 1986, 1987, 1992). Plants increase the production of hormones to create galls or abnormal growths in response to chemical and/or mechanical stimulation ⁎ Corresponding author at: Richard Gilder Graduate School at the American Museum of Natural History, 79th at Central Park West, New York City, New York 10024, USA. E-mail addresses: [email protected] (A.R. Holden), [email protected] (D.M. Erwin), [email protected] (K.N. Schick), [email protected] (J. Gross).
from invaders such as bacteria, fungi, mites, and insects (Mani, 1992; Labandeira, 2002; Russo, 2006). Cynipine wasps oviposit into selective, growing plant tissue. Once larvae hatch, secretions from their feeding cause the acceleration of production of plant tissue, which serves as food and shelter. In effect, the walls of the larval chamber are a nutritious layer of cells or a nutrient sink that renews as the larvae grow and feed (Dreger-Jaufret et al., 1992; Labandeira, 2002; Stone and Schönrogge, 2003, Stone and Schönrogge, 2003; Shorthouse et al., 2005; Russo, 2006). Other specialized cells on the outer layer of the gall can include tannins and starch, which may repel enemies (Dreger-Jaufret and Shorthouse, 1992; Russo, 2006). Among gall insects, cynipines form the most structurally complex and varied galls, including both unilocular (single-chambered) and multilocular (multi-chambered) types that are often diagnostic at the species level (Rohfritsch, 1992; Stone and Schönrogge, 2003; Csóka et al., 2005; Russo, 2006; Bailey et al., 2009). The oak gall wasps (Hymenoptera: Cynipidae: Cynipini) comprise over 940 species worldwide and are only surpassed by gall midges (Diptera: Cecidomyiidae) as the most common gall insect (Felt, 1940; Dreger-Jaufret and Shorthouse, 1992). According to Roskam (1992), Cynipini arose 25 million years ago in the Miocene. However, Rasnitsyn and Quicke (2002) assign their putative age to the Late Cretaceous. The fossil-calibrated divergence estimate of Buffington et al.
http://dx.doi.org/10.1016/j.yqres.2015.09.008 0033-5894/© 2015 University of Washington. Published by Elsevier Inc. All rights reserved.
Please cite this article as: Holden, A.R., et al., Late Pleistocene galls from the La Brea Tar Pits and their implications for cynipine wasp and native plant distribution in souther..., Quaternary Research (2015), http://dx.doi.org/10.1016/j.yqres.2015.09.008
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(2012) suggest Cynipini arose approximately 50 million years ago, and the deeper split between the phytophagous cynipids and entomophagous figitids is dated to approximately 125 million years ago, give or take 25 million years. Most gall wasps within Cynipini are associated with Quercus spp.; their distribution and diversity concurs with that of oaks, regarded as the dominant tree species in temperate, deciduous forests in the Northern Hemisphere at the beginning of the early Paleogene (Roskam, 1992). A much smaller proportion of cynipid species, in tribes other than Cynipini, are associated with dicotelydonous angiosperms, while others are inquilines in galls induced by other species (Roskam, 1992; Ronquist, 1999). Larew (1987, 1992) compiled the fossil record of cynipine oak galls, which has also been reviewed by Waggoner and Poteet (1996), Waggoner (1999), Erwin and Schick (2007) and recently by Knor et al. (2013). The first galls definitely attributed to cynipines are at least 20 million years old (Straus, 1977; Scott et al, 1994; Dieguez et al., 1996; Waggoner and Poteet, 1996; Waggoner, 1999). Larew (1986, 1987, 1992) noted that one of the weaknesses in the fossil record of galls is a general incompleteness and unexplained lack of material from the Quaternary (1992). Recent publications have begun to fill in those gaps for cynipine oak galls (Erwin and Schick, 2007) and include additional records for the Quaternary (Stone et al., 2008; Knor et al., 2013). Only two galls from Rancho La Brea have been previously reported. Larew (1987) described the acorn galls of Callirhytis milleri Weld (= C. flora Weld), a species that galls the acorns and petioles of Quercus agrifolia Née, Q. wislizenii A.DC, and Q. kellogii Newb. (all black oaks) (Weld, 1957). Callirhytis milleri is now known to be the alternate bisexual generation of C. flora Weld, a species that galls the petioles of Q. agrifolia, Q. wislizeni, and Q. kelloggii (Weld, 1957). This is a scarce record of fossil cynipine galls considering that three species of oak, Quercus dumosa Nutt., Q. lobata Née, and Q. agrifolia, have been identified from the tar pits (Templeton, 1964; Stock and Harris, 1992) and are known to host more gall-inducing organisms than any other plant, including dozens of cynipine species (Dreger-Jaufret and Shorthouse, 1992; Russo, 2006). However, Larew (1992) noted that many galls have probably remained unnoticed in paleobotany collections, no doubt because of their morphological similarities to certain plant organs. Thus, we first began our focused effort to locate galls by examining curated fruits and seeds in the George C. Page Museum botany collection. Subsequently, we studied unidentified bulk plant material from past and recent excavations. Most of the specimens we identified are virtually intact, although some have suffered slight surface abrasion and/or change in color due to asphalt saturation. A few galls were partial or fragmented. Only two species of insects identified from Rancho La Brea are considered to be extinct (scarab beetles that likely specialized on the dung of extinct mammals); all other recovered species are said to be identical to or conspecific with extant taxa (Miller et al., 1981; Miller, 1983; Stock and Harris, 1992). More generally, many researchers have observed that virtually all Quaternary insects are identical to modern species, which has stimulated a resurgent interest in their systematics and use as paleoenvironmental indicators (Miller, 1983; Elias, 1994; Coope, 2004). In light of this and evidence that cynipines have conserved plant hosts over the last 20 million years (Stone et al., 2009), our procedure was to identify fossils using modern gall morphology. Materials and methods Specimens from Pits A and 3 were excavated between 1913 and 1929. These pits are separate asphaltic deposits located in Hancock Park, a mid-city region within Los Angeles, California; fossil material was cleaned with kerosene and xylol to remove asphalt and substrate, resulting in individually separated specimens with clearly visible detail. Specimens from Pit 3 were found within the skull cavity of a sabertooth cat. The rest of the material studied was excavated from Boxes 1, 5B, 11,
and 14, which represent different asphaltic deposits from Project 23, an ongoing excavation of 16 asphaltic fossiliferous deposits along the western edge of the La Brea Tar Pits. The deposits were exposed, crated into 23 wooden boxes, and transported to a nearby compound for examination. Apart from specimens from 5B, found compacted inside a Camelops hesternus Leidy skull, all identified gall fossils were located in bulk matrix surrounding bones. The fossils were carefully extracted, soaked in Gentech N-propyl bromide to dissolve asphalt, then rinsed with water, resulting in completely separated specimens. Specimens from Rancho La Brea, California Academy of Sciences, and the Essig Museum of Entomology at the University of California, Berkeley were photographed with a Canon EOS 7D digital camera using MP-E 65 mm or 100 mm macro lenses with an attached MT-24EX Macro Twin Lite flash. Specimens from the American Museum of Natural History were photographed with a Visionary Digital photomicrographic apparatus with Infinity optics and Canon EOS 7D. All of the above images were processed using Adobe Photoshop CS6 Extended. Some of the material was radiographed using a Faxitron cabinet x-ray, model 43855C, printed on Kodak M125 Industrex film, and developed in a darkroom using photographic chemicals to determine the location and orientation of larval chambers. The radiographs were placed on a light box and photographed with a Cannon EOS Rebel XSi 450D with an EF-260 mm f/2.8 Macro USM lens. Images were processed with Adobe Photoshop CS5 to allow for higher-resolution examination. Integral stem galls with similar external morphology were CT scanned to aid in identification of fossil material by analyzing location and orientation of larval chambers, which were then compared to radiographs of fossil material. Scanning was performed on a GE Phoenix vtomex s 240 at 60 kV and 180 μA for 5-second exposures. Resulting images were 4 × 4 μm per pixel in resolution, stitched together in Image J v1.45 and rendered in Volume Graphics Studio Max v2.2. All fossil specimens are housed at the George C. Page Museum, a branch of the Natural History Museum of Los Angeles County. Cynipine gall morphology is often species-specific and therefore can be firmly attributed without observation of the insect responsible (Rohfritsch, 1992; Stone and Schönrogge, 2003; Csóka et al., 2005; Russo, 2006; Bailey et al., 2009). Visual comparisons of material, as well as radiographs and CT scans, were made using the L.H. Weld Collection of galls at the California Academy of Sciences in San Francisco, specimens from the Essig Museum of Entomology at the University of California, Berkeley, the American Museum of Natural History, and personal observations (A.R.H., D.M.E, K.N.S, and J.G.) of cynipine galls in the field. Systematic paleontology Order HYMENOPTERA Linnaeus, 1758 Superfamily CYNIPOIDEA Ashmead, 1899 Family CYNIPIDAE Westwood, 1840 Tribe CYNIPINI Ashmead, 1903 Genus DIASTROPHUS Hartig, 1840 cf. Diastrophus niger Bassett, 1900 Material. – LACMHC 475B. Description. – LACMHC 475B is a multilocular, cylindrically shaped, possibly integral stem gall that is 6.4 mm long and 3.7 mm wide. There are no remains of the stem preserved. The gall is composed of at least five larval chambers that are up to 2.5 mm wide, with some chambers showing circular exit holes (Figure 1A–C.). There is very little tissue separating what appear to be relatively simple chambers, a character apparent in modern D. niger galls (Figure 1D–F). Occurrence. – Late Pleistocene. Rancho La Brea Tar Pits, Pit A. Remarks. – This gall is slim, stem-like, with few cells and has a general lumpy external morphology (unlike linear D. fragariae Beutenmuller), as if the petiole layer had worn away. Host. – Cinquefoil (Potentilla). Diastrophus sp.
Please cite this article as: Holden, A.R., et al., Late Pleistocene galls from the La Brea Tar Pits and their implications for cynipine wasp and native plant distribution in souther..., Quaternary Research (2015), http://dx.doi.org/10.1016/j.yqres.2015.09.008
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Fig. 1. Diastrophus niger. A–C) LACMHC 475B. Scale bar equals 1 mm. D, F) Modern material. Scale bar equals 5 mm. E) CT scan cross-section of F. Scale bar equals 2 mm.
Material. – LACMHC 470Ba (Figure 2A–C), 470Bb (Figure 2A), LACMP23 11092 (Figure 2D–F). Description. – LACMHC 470Ba and b are parts of a single multilocular stem gall. There is very little tissue between the larval chambers, which are held together by thin sheaths of tissue. LACMHC 470Bb is tapered at one end and widens toward the other (viz.) teardrop shaped. The complete gall is 8.0 mm long and 5.0 mm wide, and shows the possible remnant of a slender stem at the narrow end of the gall (Figure 2B, C). There are about seven chambers, which are each about 3 mm in their longest dimension. In places where the chamber walls are broken, these walls are notably thin. The chambers abut one another and their shapes vary. LACMP23 11092 is another fragment of a multilocular gall similar to LACMHC 470Ba and b (Figure 2D–F). This specimen is 6.0 mm long and 3.4 mm wide. It has six to seven chambers that are 2.0–2.5 mm wide, and there are two exit holes (Figure 2D).
Occurrence. – Late Pleistocene. Rancho La Brea Tar Pits. LACMHC 470Ba and 470Bb are from Pit A; LACMP23 11092 is from Project 23, Box 5B. Remarks. – Diastrophus is distinguished from other cynipid galls by simplest structure and little tissue specialization. Host. – Rosaceous hosts such as Cinquefoil (Potentilla), brambles (Rubus), and wild strawberry (Fragaria). Genus NEUROTERUS Hartig, 1840 cf. Neuroterus cupulae Kinsey, 1922 Material. – LACMP23 11112 (Figure 3A, B). Description. – LACMP23 11112 is the remains of a small, partial acorn cap (involucre), 4.6 mm wide and 2.2 mm high, covered with tiny, overlapping triangular scales, 0.7 mm wide near their base and 0.8 mm long (Fig. 3A, B). This specimen shows two circular holes (Figure 3 A, B). The interior hole is 0.7 mm wide (Figure 3B) and the other smaller exterior hole is 0.5–06 mm wide (Figure 3A). The exterior hole represents an exit
Fig. 2. Diastrophus sp. A) 470Ba, 470Bb. B, C) LACMHC 470Ba. D-F) LACMP23 11092.
Please cite this article as: Holden, A.R., et al., Late Pleistocene galls from the La Brea Tar Pits and their implications for cynipine wasp and native plant distribution in souther..., Quaternary Research (2015), http://dx.doi.org/10.1016/j.yqres.2015.09.008
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Fig. 3. Neuroterus cupulae. A, B) LACMP23 11112, with exit hole and (B) with larval chamber. Scale bar equals 2 mm. C, D) Modern material, with larval chambers and exit holes. Scale bar equals 5 mm.
hole located in the cap. Internal to the external hole and lying below the floor of the nut, there is a cavity that appears to be a former larval chamber (Figure 3B). The relationship of the larger internal hole to the nut or chamber lying below it is not clear. Similar larval chambers and exit holes are visible in modern, comparative material (Figure 3C, D). Occurrence. – Late Pleistocene. Rancho La Brea Tar Pits, Project 23, Box 11. Remarks. – It cannot be entirely ruled out that an acorn-feeding weevil produced the exit hole. Host. – Valley oak (Q. lobata ), (Kinsey and Ayres, 1922), coastal sage scrub oak (Q. dumosa), and blue oak (Q. douglasii Hook. and Arn.). Genus ANDRICUS Hartig, 1840 Andricus occultatus Weld, 1926 Material. – LACMHC 479B. Description. – LACMHC 479B is a tiny bud gall, 2.8 mm long and 1.6 mm wide (Figure 4A). The gall is laterally compressed and consists of a small circular base, 0.8 mm wide, and with over 20 minute imbricate scales, the basal ones measuring about 1.0 mm, decreasing in size apically (Figure 4A). There is a well-defined exit hole, about 0.4 mm
Fig. 4. Andricus occulatus. A) LACMHC 479B, with exit hole. Scale bar equals 1 mm. B) Modern material, with exit hole. Scale bar equals 1mm.
wide, located in the mid-region on the flattened side of the gall (Figure 4A). Occurrence. – Late Pleistocene. Rancho La Brea Tar Pits, Pit A. Remarks. – LACMHC 479B is virtually indistinguishable from modern material; the size and morphology of the bud and exit hole are the same as extant examples of this species (Figure 4B). Host. –White oaks, which include valley oak (Q. lobata), leather oak (Q. durata Jep.), Nuttall's scrub oak (Q. dumosa), scrub oak (Q. berberidifolia Liebm.), blue oak (Q. douglasii), and Oregon oak (Q. garryana Doug. ex Hook.). Genus BESBICUS Kinsey, 1930 cf. Besbicus conspicuus Kinsey, 1930 Material. – LACMP23 11106. Description. – The specimen has a smooth, strongly rugose surface pattern (Figure 5A, B). It is 6.6 mm at its widest diameter, and the shortest is 5.8 mm (Figure 5A, B). The radiograph (Figure 5C) shows a single, central chamber surrounded by tissue. Occurrence. – Late Pleistocene. Rancho La Brea Tar Pits, Project 23, Box 11. Remarks. – Similar to the unilocular galls of Besbicus conspicuous (Figure 5C, D). This species is mislabeled as Disholcaspis washingtonensis Gillette in Russo (2006). Host. – Pacific white oaks, which include blue oak (Q. douglasii), deer oak (Q. sadleriana Brown), Engelmann oak (Q. engelmannii Greene), leather oak (Q. durata), Nuttall's scrub oak (Q. dumosa), scrub oak (Q. berberidifolia), and valley oak (Q. lobata) (Russo, 2006). Genus DISCHOLCASPIS Dalla Torre and Kieffer, 1910 cf. Disholcaspis prehensa Weld, 1957 Material. – LACMHC 477B (Figure 6A–C) and LACMP23 13422 (Figure D–F). Description. – Both specimens are reminiscent of the multilocular stem galls of Disholcaspis prehensa. LACMHC 477B has a flared base 7.0 mm wide and the gall is 6.5 mm tall (Figure 6A–C). The apical cap area is circular, 4.0 mm wide and 0.8 mm thick (Figure 6A–C). A rim (carina) encircles the base of the cap where it attaches to the main body of the gall (Figure 6A–C). The cap surface is rugose and divided into small wedges (Figure 6B). The tissue of the main gall body has a rough, degraded texture (Figure 6A–C). LACMP23 13422 is approximately 6.0 mm wide and has an ovoid rugose cap, 2.3 mm wide and 0.7 mm thick (Figure 6D–E). Portions of the sides of the main gall body are flaking off; the outer layer is thin and appears to have separated from the inner spongy tissue of the gall wall (Figure 6D). Occurrence. – Late Pleistocene. Rancho La Brea Tar Pits. LACMHC 477B is from Pit A; LACMP23 13422 is from Project 23, Box 1. Remarks. – While portions of the specimens have exfoliated, enough remains to discern their resemblance to D. prehensa (Figure 6F). Host. – Pacific white oaks, which include blue oak (Q. douglasii), deer oak (Q. sadleriana), Engelmann oak (Q. engelmannii), leather oak (Q. durata), Nuttall's scrub oak (Q. dumosa), scrub oak (Q. berberidifolia), and valley oak (Q. lobata) (Russo, 2006). Genus DRYOCOSMUS Giraud, 1859 cf. Dryocosmus dubiosus Material. – LACMP23 12854. Description. – This specimen (Figure 7A–D) resembles the unilocular leaf galls of D. dubiosus (Figure 7E, F). The specimen is boat-shaped and measures 3 mm long and 1.5 mm wide. There is a minute circular hole, 0.10 mm wide, located on the underside of the specimen; this may be an exit hole (Figure 7C, D). Occurrence. – Late Pleistocene. Rancho La Brea Tar Pits, Project 23, Box 1. Remarks. – Similar to the extant gall (Figure 7 E, F) but also resembles Arctostaphylos seeds and hole may be predation. Host. – Black oaks including California black oak (Q. kellogii), coast live oak (Q. agrifolia), and interior live oak (Q. wislizenii ) (Russo, 2006). Genus CALLIRHYTIS Förster, 1869
Please cite this article as: Holden, A.R., et al., Late Pleistocene galls from the La Brea Tar Pits and their implications for cynipine wasp and native plant distribution in souther..., Quaternary Research (2015), http://dx.doi.org/10.1016/j.yqres.2015.09.008
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Fig. 5. Besbicus conspicuus. A–C) LACMP23 11106. C) Radiograph of LACMP23 11106. Scale bar equals 2 mm. D, E) Modern material, whole and cross-sectioned. Scale bar equals 2 mm.
c.f. Callirhytis quercussuttoni (Basset) Dalla Torre and Kieffer, 1910 Andricus quercussuttoni (Dalla Torre and Keiffer) Melika and Abrahamson, 2002) Material. – LACMHC 430B (Figure 8A–C) and LACMHC 431Bb (Figure 8D–F). Description. – LACMHC 430B is a multilocular integral stem gall resembling the extant galls of Callirhytis quercussuttoni (Figure 8A-H). It is ovoid in shape, 1.5 cm long by 1.0 cm wide, with the stem visibly running through the gall and portions of it sticking out at each end (Figure 8A–C). The gall is somewhat asymmetrical in being flattened on one side with the stem not running through the center of the gall (Figure 8B). No larval chambers are visible on the flattened side the gall (Figure 8B). Four exit holes, approximately 0.8 mm diameter, with distinctive rims are visible and correspond to the underlying larval chambers (Figure 8A). Though not exceptionally clear, the radiograph does appear to show the chambers are separated by tissue (Figure 8C). CT scans (Figure 8G) also show chambers separated by tissue but sometimes closely abutting. LACMHC 431Bb is a multilocular, integral stem gall (Figure 8D–F). It is ovoid measuring 2.1 cm long and 1.5 cm wide, with a short remnant of its narrow 3.0 mm wide branch, still attached (Figure 8D, E). On one side of the specimen, a couple of pieces have broken off exposing the interior of the gall revealing the larval chambers (Figure 8D, E). Larval chambers are 2.0–2.5 mm wide with openings that may be exit holes. This gall is pear-shaped and slightly beaked (Figure 8D, E). There are at least 15 chambers visible in the exposed area. On the unbroken surface, there is evidence of larval chamber position and exit holes, which are infilled with asphalt (Figure 8D). In surface view, there appears to be tissue between the chambers, but the radiograph shows there is very little tissue separating the chambers (Figure 8E). The chambers are numerous, closely spaced, and the inclosing cavities somewhat angular in section view (Figure 8E). Occurrence. – Late Pleistocene. Rancho La Brea Tar Pits, Pit A. Remarks. – Diagnostic to species-level features include tissue in between cells (Figure 8C–G), exit holes on outside (Figure 8A, H), rim around exit holes (Figure 8A, H), stem tissue in between (Figure 8A, B, D, E), cells oriented around stem (Figure 8C), cells oriented in the same direction (Figure 8F). Russo (2006) describes these galls as
forming abruptly on the stems, suggesting there is little taper where the gall and stem meet. Though many C. quercussuttoni galls do show little taper at the gall-stem junction, some are more tapered. In A. spectabilis Kinsey or Dryocosmus asymmetricus Kinsey the stems are typically more tapered at the gall-stem juncture. However, some C. quercussuttoni galls do have stems that taper at the gall-stem juncture. LACMHC 431Bb also shows some similarity to A. spectabilis, which has external exit holes, chambers oriented toward gall surface so exit holes directly face outward, and there is tissue between the chambers. However, there is also some similarity to modern D. asymmetricus, which shows very little tissue separating larval chambers. Host. – Black oaks, which include California black oak (Q. kellogii), coast live oak (Q. agrifolia), and interior live oak (Q. wislizenii) (Russo, 2006). cf. Callirhytis quercuspomiformis Bassett, 1881 (Amphibolips quercuspomiformis (Bassett) Melika and Abrahamson, 2002) Material. – LACMHC 431Ba. Description. – This specimen is a woody, multilocular detachable stem gall (Figure 9A–C). It is asymmetrically shaped, rounded on one side and flattened on the other (Figure 9A–C). It measures 13.4 mm long, 9.9 mm tall and 10.5 mm wide, and contains at least 20 chambers, with roughly circular outlines (Figure 9A–C). The chambers are oriented perpendicular to the long axis of the gall, arranged in a regular pattern, and with tissue in between (Figure 9A– C).) Chambers are relatively large and of various sizes as seen in different levels of section and views (Figure 9A–C). They measure 1.8–2.8 mm wide and up to 4.5 mm long (Figure 9A–C). The specimen appears to be worn and abraded, with the inner layers of the chambers no longer preserved and filled in with asphalt (Figure 9A–C). Occurrence. – Late Pleistocene Rancho La Brea Tar Pits, Pit A. Remarks. – This specimen most closely resembles the detachable stem galls of Callirhytis quercuspomiformis (Figure 9D, E. There are morphological similarities and differences to Diastrophus kincaidii Gillette, a multilocular integral stem gall found on thimbleberry (Rubus parviflorus Nutt.) such as the globular shape and radial orientation of larval cells around the stem (Russo, 2006; Weld, 1957).
Please cite this article as: Holden, A.R., et al., Late Pleistocene galls from the La Brea Tar Pits and their implications for cynipine wasp and native plant distribution in souther..., Quaternary Research (2015), http://dx.doi.org/10.1016/j.yqres.2015.09.008
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Fig. 6. Disholcaspis prehensa. A–C) LACMHC 477B, carina visible. Scale bar equals 1 mm. D, E) LACMP23 13422, carina visible, layers, other layers flaking off. Scale bar equals 1 mm. F) Modern material, approximately 10 mm wide at the base with caps about 5 mm wide.; 7–10 mm high (Russo, 2006).
Host. – Black oaks, which include California black oak (Q. kellogii), coast live oak (Q. agrifolia), and interior live oak (Q. wislizenii) (Russo, 2006). cf. UNDESCRIBED EXTANT GALL Material. – LACMHC 468B. Description – This specimen has a circular hole, most likely an exit hole, 0.4 mm wide, located on the side of the gall (Figure 10A). There is a raised knob, 0.5 mm long, 0.4 mm wide, and 0.1 mm thick on the lower surface of LACMHC 468B (Figure 10A–C). It has an ovoid shape with a somewhat irregular outline (Figure 10A–C). The area of the gall wall near the knob has fine linear striations radiating out from the base of the knob (Figure 10C). Surface of the knob appears pitted (Figure 10A–C). The surface of the main body is characterized by minute tubercles scattered over the gall surface (Figure 10A–C). Occurrence. – Late Pleistocene Rancho La Brea Tar Pits, Pit 3. Remarks. – This gall resembles extant, undescribed galls of similar size, shape, and surface structure that occur on the leaves of canyon live oak (Q. chrysolepis Liebm.) (Figure 10D–H). Host. – Possibly canyon live oak (Q. chrysolepis).
Discussion The collection of Rancho La Brea galls described here represents new records for the late Pleistocene of western North America for Callirhytis, Diastrophus, Disholcaspis, Andricus, Neuroterus, Besbicus, and Dryocosmus, as well as providing minimum probable dates and revealing an undescribed species. It also contributes to the Cenozoic fossil record of galls, especially for the Quaternary, for which few identified specimens are known (Larew, 1992). Three-dimensional fossil galls are extremely rare (Larew, 1986, 1992; Stone et al., 2008). The vast majority of galls in the fossil record are preserved as compressions, which often lack the structural complexity necessary to identify the gall maker, as well as potential host plants, parasites, and inquilines (Stone et al., 2008). Recognizing fossil galls can be a challenge and many have been mistaken for typical plant parts like cones, inflorescences, fruits, and seeds. Many nondescript holes on fossil leaves have been attributed to gallers and interpreted as sites of former gall attachments. However, discerning this type of damage from similar types caused by bacteria, fungi, leaf
Please cite this article as: Holden, A.R., et al., Late Pleistocene galls from the La Brea Tar Pits and their implications for cynipine wasp and native plant distribution in souther..., Quaternary Research (2015), http://dx.doi.org/10.1016/j.yqres.2015.09.008
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Fig. 7. Dryocosmos dubiosus, asexual, fall generation. A–D) LACMP23 12854. Scale bar equals 1 mm. C, D) Probable exit hole. E, F) Modern material of the asexual gall, variable, but similar in length.
damage due to puncturing, or other physical non-biological causes, or the feeding of phytophagous insects, is difficult. In contrast, the unique fossil preservation at the La Brea Tar Pits provides an opportunity to study three-dimensionally intact and original material, thus lending high confidence to identifications. Larew (1992) noted that many fully interpretable fossil galls may be left unnoticed in museum collections. Rancho La Brea's holdings are a good example: although a few have been recognized, prepared, and curated, this paper demonstrates that many more can be identified and described in considerable detail, given the great abundance of oak and other major gall hosts recovered there. One of the more significant aspects of this fossil gall collection is that it indicates the late Pleistocene presence of host plants that have not yet been recognized as such at Rancho La Brea based on our hypothesis of extant gall species specificity. Potential, but unrecorded, hosts include oak species such as Pacific white oak species—Blue oak (Q. douglasii), deer oak (Q. sadleriana), Engelmann oak (Q. engelmannii), leather oak (Q. durata), and scrub oak (Q. berberidifolia)—Black oaks including California black oak (Q. kellogii) and interior live oak (Q. wislizenii)—as well as Cinquefoil (Potentilla), and wild strawberry (Fragaria). The presence of these hosts offers clues to the local paleo14 environment between approximately ~2200 and 60,000 C yr BP, but with most specimens provisional dated to between ~ 30,000 and 14 48,000 C yr BP. While the La Brea galls have not been directly dated, ranges of dates on other material from these deposits have been acquired at the W. M. Keck Carbon Cycle Accelerator Mass Spectrometry Laboratory at University of California, Irvine (Fuller et al., 2014). Specific
14
intervals dated thus far include Pit A, which is ~2200 to 47,000 C yr BP; 14 Pit 3, which is ~14,000–21,000; C yr BP; Project 23 Box 1, which is from 14 ~30,000 C yr BP to older than can be measured with radiocarbon dat14 ing, but with a high proportion of dates between 35,000 and 37,000 C 14 yr BP; 5B, which is ~42,000–47,000 C yr BP; Box 11, which has one date 14 at 37,000 C yr BP; and the range for Box 14 , which is ~42,000–48,000 14 C yr BP (Fuller et al., 2014; J.R. Southon, pers. comm.). All of the Rancho La Brea gall-forming cynipines are evidently extant. Each indicates the presence of a host plant with known, modern current climatic range. Thus these fossil data could provide new insights concerning late Ice Age environmental conditions prevailing in southern California. However, there are caveats. The host plants identified on the basis of fossil galls occur in a diverse range of habitats in present-day California. These environments include coniferous forest, mixed evergreen, woodlands–savannah, and chaparral (Munz and Keck, 1959; Ordnuff et al., 2003; Baldwin et al., 2012). Among these habitats, the average precipitation currently ranges from as little as approximately 35 to as much as 280 cm per year (Munz and Keck, 1959; Ordnuff et al., 2003); the average winter minimum is as low as − 1.6°C and the average summer maximum is as high as 35°C (Munz and Keck, 1959; Ordnuff et al., 2003); and host plants presently occur in elevations ranging from approximately 45–760 m (Baldwin et al., 2012). Given such an implausibly large range of ecological conditions during a narrow time interval at Rancho La Brea, supported by the aforementioned, wide provisional date ranges for the galls, the only plausible conclusion is that some gall specimens found there in fact originated elsewhere, and were secondarily deposited by fluviatile conditions and alluvial wash (Shaw and Quinn,
Please cite this article as: Holden, A.R., et al., Late Pleistocene galls from the La Brea Tar Pits and their implications for cynipine wasp and native plant distribution in souther..., Quaternary Research (2015), http://dx.doi.org/10.1016/j.yqres.2015.09.008
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Fig. 8. Callirhytis quercussuttoni. A–C) LACMHC 430B. Scale bar equals 5 mm. A) Exit holes surrounded by round, flat rim. A, B, D, E) Stem visible. C) Radiograph shows chambers separated by tissue. D–F) LACMHC 431Bb. Scale bar equals 5 mm. D) Chamber separated by tissue. D–E) Exposed chambers, branch visibly attached. F) Radiograph shows little tissue separating chambers. G) CT scan cross-section of H (modern material). Both with scale bar equal to 5 mm. H) Exit holes with flat rims.
1986). Possibly, the abraded specimens represent transportation from such nonlocal habitats, although abrasion could also occur in the case of asphaltic movement within tar pits, whereas the more intact specimens were dropped in situ at Rancho La Brea.
Although the fossil gall collection described in this paper is of limited value for interpreting paleocological conditions in the immediate environs of Rancho La Brea, it has much significance nevertheless. Assuming that ecological conditions required by native plants in California during
Fig. 9. Callirhytis quercuspomiformis, asexual, summer generation. A–C) LACMHC 431Ba, chambers oriented perpendicular to long axis of the gall, arranged in regular pattern, and with tissue in between. Scale bar equals 5 mm. D, E) Modern material, with similar chamber orientation around stem. Scale bar equals 1 cm.
Please cite this article as: Holden, A.R., et al., Late Pleistocene galls from the La Brea Tar Pits and their implications for cynipine wasp and native plant distribution in souther..., Quaternary Research (2015), http://dx.doi.org/10.1016/j.yqres.2015.09.008
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Fig. 10. Undescribed gall. A–C) Exit hole, bottom knob, and adjacent striations. Scale bar equals 0.5 mm. D–H) Similar surface structure, shape, knob. Scale bar equals 0.5 mm.
the late Pleistocene were the same as those prevailing today, the taxonomic diversity of the fossil galls indicates that almost every habitat in the state today existed during the late Pleistocene. Does this, in turn, imply that regional plant communities have not drastically changed since the late Pleistocene? This has been suggested by some studies on Rancho La Brea plant fossils (Templeton, 1964; Warter, 1976). Currently, Rancho La Brea plant fossils have been used to reconstruct four plant associations: chaparral, coastal sage scrub, deep canyon, and riparian (Shaw and Quinn, 1986; Stock and Harris, 1992). While many of the fossil gall hosts fit within these groups, new host records, including Quercus kellogii, sadleriana, wislizenii, and garrayana, as well as Rubus parviflorus, are consistent with the kinds of mesic ecological conditions found at elevations higher than those preferred by the current coastal sage scrub community (Holden et al., 2014). By the same token, the occurrence of gall-forming insects that thrive in hot and even arid conditions (Holden et al., 2013) is also discordant with conditions prevailing at Rancho La Brea today. Clearly, original provenance and age are all-important: only when the content of the local fossil entomofauna is firmly established for Rancho La Brea, in sufficient abundance to permit destructive sampling, will a clear understanding of ecological change and continuity at Rancho La Brea emerge (Shaw and Quinn, 1986; Holden et al., 2014). In closing, we emphasize that La Brea cynipine galls are fossils of substantial but undervalued significance. Not only do they permit identification of hosts otherwise unknown, they may also provide evidence for the occurrence of other fossils of great interest, such as potential inquilines, parasites, parasitoids, predators, and even fungi that form the micro-communities of complex galls (Mani, 1992; Csóka et al., 2005; Stone et al., 2008). Rancho La Brea's lesser known yet immense insect and plant collections are a storehouse of data for reconstructing regional late Pleistocene climate, habitats, flora, and vegetation—when dated, these insect communities can potentially provide a high-resolution snapshot of the prehistoric paleoenviroment of the Rancho La Brea Tar Pits and the conditions that provided food, shelter, and other necessities of life for the doubtlessly charismatic, but nonetheless utterly dependent, megafauna.
Acknowledgments We thank the following individuals: From the American Museum of Natural History—J. Carpenter and R. MacPhee provided review, and C. Lebeau provided access to comparative material; S. Tucker provided many photographic images; M. Hill, H. Towbin, and P. Barden coordinated and assisted in CT scanning; funding from the Museum supported this project. George C. Page Museum—J. Harris offered financial support; S. Cox, A. Farrell, G. Takeuchi, and T. Valle expedited the preparation and documentation of specimens for the study and provided information on specimen excavation and provenance; C. Howard provided many photographic images for research and publication; L. Tewksbury, C. Howard, M. Tabencki, K. Rice, and C. Lutz were involved in Project 23 excavation. From the Natural History Museum of Los Angeles County—L. Chiappe provided review and guidance, and R. Hulser assisted with references; funding from the Museum supported this project. From the University of California, Irvine— J. Southon, B. Fuller, and S. Fahrni provided dates of specimens within Project 23 deposits. From the United States Department of Agriculture—M. Buffington provided extensive review. We also thank G. Csóka, S. Elias, B. R. Barton, and A. Gillespie for their constructive review. References Bailey, R., Schönrogge, K., Cook, J.M., Melika, G., Csóka, G., Thuróczy, C., Stone, G.N., 2009. Host niches and defensive extended phenotypes structure parasitoid wasp communities. PLoS Biol. 7 (8), e1000179. Baldwin, B.G., Goldman, D.H., Keil, D.J., Patterson, R., Thomas, J.R., 2012. The Jepson Manual. Vascular plants of California, Second edition University of California Press, Berkeley, Los Angeles, and London. Buffington, M.L., Brady, S.G., Morita, S.I., Van Noort, S., 2012. Divergence estimates and early evolutionary history of Figitidae (Hymenoptera: Cynipoidea). Syst. Entomol. 37 (2), 287–304. Coope, G.R., 2004. Several millions of year of stability among insect species because of, or in spite of, Ice Age climatic instability? Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 359, 209–214. Csóka, G., Stone, G.N., Melika, G., 2005. Biology, ecology and evolution of gall-inducing Cynipidae. In: Raman, A., Schaefer, C.W., Withers, T.M. (Eds.), Biology, Ecology and Evolution of Gall-Inducing Arthropods. Science Publishers, Enfield, pp. 573–642. Dieguez, C., Nieves-Aldrey, J.L., Barron, E., 1996. Fossil gall (zoocecids) from the Upper Miocene of La Cerdana (Lerida, Spain). Rev. Palaeobot. Palynol. 94, 329–343.
Please cite this article as: Holden, A.R., et al., Late Pleistocene galls from the La Brea Tar Pits and their implications for cynipine wasp and native plant distribution in souther..., Quaternary Research (2015), http://dx.doi.org/10.1016/j.yqres.2015.09.008
10
A.R. Holden et al. / Quaternary Research xxx (2015) xxx–xxx
Dreger-Jaufret, F., Shorthouse, J.D., 1992. Diversity of gall inducing insects and their galls. In: Shorthouse, J.D., Rohfritsch, O. (Eds.), The Biology of Insect-Induced Galls. Oxford University Press, New York, Oxford, pp. 8–33. Elias, S.A., 1994. Quaternary Insects and Their Environments. Smithsonian Institution Press, Washington D.C. Erwin, D.M., Schick, K.N., 2007. New Miocene oak galls (Cynipini) and their bearing on the history of cynipid wasps in western North America. J. Paleontol. 81 (3), 568–580. Felt, E.P., 1940. Plant Galls and Gall Makers. Comstock Publishing Company, Ithaca, New York. Fuller, B.T., Fahrni, S.M., Harris, J.M., Farrell, A.B., Coltrain, J.B., Gerhart, L.M., Ward, J.K., Taylor, R.E., Southon, J.R., 2014. Ultrafiltration for asphalt removal from bone collagen for radiocarbon dating and isotopic analysis of Pleistocene fauna at the tar pits of Rancho La Brea, Los Angeles, California. Quat. Geochronol. 22, 85–98. Holden, A.R., Harris, J.M., Timm, R.M., 2013. Paleoecological and taphonomic implications of insect-damaged Pleistocene vertebrate remains from Rancho La Brea, southern California. PloS One 8 (7), e67119. Holden, A.R., Koch, J.B., Griswold, T., Erwin, D.M., Hall, J., 2014. Leafcutter bee nests and pupae from the Rancho La Brea Tar Pits of southern California: Implications for understanding the paleoenvironment of the Late Pleistocene. PloS One I (4), e94724. Kinsey, A.C., Ayres, K.D., 1922. Studies of Some New and Described Cynipidae (Hymenoptera). University of Indiana, Bloomington. Knor, S., Skuhrava, M., Wappler, T., Prokop, J., 2013. Galls and gall makers on plant leaves from the lower Miocene (Burdigalian) of the Czeck Republic: systematic and paleoecological implications. Rev. Palaeobot. Palynol. 188, 38–51. Labandeira, C.C., 2002. The history of associations between plants and animals. In: Herrera, C.M., Olle, P. (Eds.), Plant-Animal Interactions: An Evolutionary Approach. John Wiley and Sons, Hoboken, New Jersey, pp. 26–76. Larew, H.G., 1986. The fossil gall record: a brief summary. Proc. Entomol. Soc. Wash. 88, 385–388. Larew, H.G., 1987. Two cynipid wasp acorn galls preserved at the La Brea Tar Pits (early Holocene). Proc. Entomol. Soc. Wash. 89 (4), 831–833. Larew, H.G., 1992. Fossil galls. In: Shorthouse, J.D., Rohfritsch, O. (Eds.), The Biology of Insect-Induced Galls. Oxford University Press, New York, Oxford, pp. 50–59. Mani, M.S., 1992. Introduction to cecidology. In: Shorthouse, J.D., Rohfritsch, O. (Eds.), The Biology of Insect-Induced Galls. Oxford University Press, New York, Oxford, pp. 3–7. Miller, S.E., 1983. Late Quaternary insects of Rancho La Brea and McKittrick, California. Quat. Res. 20 (1), 90–104. Miller, S.E., Gordon, R.D., Howden, H.F., 1981. Reevaluation of Pleistocene scarab beetles from Rancho La Brea, California (Coleoptera: Scarabaeidae). Proc. Entomol. Soc. Wash. 83, 625–630. Munz, P.A., Keck, D.D., 1959. A California Flora. University of California Press, Berkeley and Los Angeles.
Ordnuff, R., Fabert, P.M., Wolf, T.K., 2003. Introduction to California Plant Life. University of California Press, Berkeley. Rasnitsyn, A.P., Quicke, D.L. (Eds.), 2002. History of Insects. Kluwer Academic Publishers, Norwell, Massachusetts. Rohfritsch, O., 1992. Patterns in gall development. In: Shorthouse, J.D., Rohfritsch, O. (Eds.), The Biology of Insect-Induced Galls. Oxford University Press, New York, Oxford, pp. 60–86. Ronquist, F., 1999. Phylogeny, classification and evolution of the Cynipoidea. Zool. Scr. 28 (1‐2), 139–164. Roskam, J.C., 1992. Evolution of the gall-inducing guild. In: Shorthouse, J.D., Rohfritsch, O. (Eds.), The Biology of Insect-Induced Galls. Oxford University Press, New York, Oxford, pp. 34–49. Russo, R., 2006. Field Guide to Plant Galls of California and Other Western States. University of California Press, Berkeley and Los Angeles. Scott, A.C., Stephenson, J., Collinson, M.E., 1994. The fossil record of leaves with galls. In: Williams, M.A.J. (Ed.), Plant GallsSystematics Association Special Volume No. 49. Clarenson Press, Oxford, pp. 447–470. Shaw, C.S., Quinn, J.P., 1986. Rancho La Brea: a look at coastal southern California's past. Calif. Geol. 39, 123–133. Shorthouse, J.D., Wool, D., Raman, A., 2005. Gall-inducing insects—nature's most sophisticated herbivores. Basic Appl. Ecol. 6 (5), 407–411. Stock, C.S., Harris, J.M. (Eds.), 1992. Rancho La Brea: A Record of Pleistocene Life in California. Natural History Museum of Los Angeles County, Los Angeles, California. Stone, G.N., Schönrogge, K., 2003. The adaptive significance of insect gall morphology. Trends Ecol. Evol. 18, 512–522. Stone, G.N., van der Ham, R.W.J.M., Brewer, J.G., 2008. Fossil oaks preserve ancient multitrophic interactions. Proc. R. Soc. Lond. B Biol. Sci. 275, 2213–2219. Stone, G.N., Hernandez‐Lopez, A., Nicholls, J.A., Di Pierro, E., Pujade‐Villar, J., Melika, G., Cook, J.M., 2009. Extreme host plant conservatism during at least 20 million years of host plant pursuit by oak gallwasps. Evolution 63 (4), 854–869. Strauss, A., 1977. Gallen, Minen und andere Fraßspuren in Pliozän von Willershausen am Harz. Verhandlungen der Botanischen Vereins der Provinz Badenburg 113, 43–80. Templeton, B.C. 1964. The fruits and seeds of the Rancho La Brea Pleistocene deposits: Oregon State University, Unpublished PhD dissertation. Waggoner, B.M., 1999. Fossil oak leaf galls from stinking water paleoflora of Oregon (middle Miocene). PaleoBios 19 (3), 8–14. Waggoner, B.M., Poteet, M.F., 1996. Unusual oak leaf galls from the middle Miocene of northwestern Nevada. J. Paleontol. 70, 1080–1084. Warter, J.K., 1976. Late Pleistocene plant communities—evidence from the Rancho La Brea Tar Pits. Symposium proceedings on plant communities of southern California. Calif. Native Plant Soc. Spec. Pub. volume 2, pp. 32–39. Weld, L.H., 1957. Cynipid galls of the Pacific slope. Privately Printed.
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Late Pleistocene galls from the La Brea Tar Pits and their implications for cynipine wasp and native plant distribution in southern California Anna R. Holden a,b,c,⁎, Diane M. Erwin d, Katherine N. Schick e, Joyce Gross f a
Richard Gilder Graduate School at the American Museum of Natural History, 79th at Central Park West, New York City, NY 10024, USA Department of Entomology, Natural History Museum of Los Angeles County, 900 Exposition Boulevard, Los Angeles, CA 90007, USA La Brea Tar Pits and Museum, 5801 Wilshire Boulevard, Los Angeles, CA 90036, USA d Museum of Paleontology, University of California, Berkeley, CA 94720, USA e Essig Museum of Entomology, University of California, Berkeley, CA 94720, USA f Berkeley Natural History Museums, University of California, Berkeley, CA 94720, USA b c
a r t i c l e Article history: Received 6 May 2015 Available online xxxx Keywords: Paleoenvironment Cynipine Gall Rancho La Brea Pleistocene
i n f o
a b s t r a c t Thirteen intact cynipine galls (Cynipidae) are identified from the significant late Pleistocene locality of Rancho La 14 Brea, mostly within the range of approximately 30,000 to 48,000 C yr BP. Late Cenozoic cynipids have a poor fossil record; it is thus of great interest that the provisional dates for this fossil gall collection establish that these insects and their hosts were an important part of the late Pleistocene ecosystem in and around Rancho La Brea. Cynipine host specificity both verifies, as well as augments, the proportionally low record of plants recovered at Rancho La Brea in comparison to records of mammals, birds, and other fauna. Because galler and hosts represent extant species, their climate and habitat restrictions offer a good basis for making paleoecological inferences. In particular, they imply that many of the diverse habitats found in California today, or, at least plant associations with similar environmental restrictions, some presently a distance from the Rancho La Brea Tar Pits, existed in the vicinity of this locality during the late Pleistocene. This material also includes previously undescribed species, several of which are morphologically similar to extant comparative material that exhibits a “jumping” behavior, previously believed to be unique to Neuroterus saltatorius Edwards. © 2015 University of Washington. Published by Elsevier Inc. All rights reserved.
Introduction The Rancho La Brea Tar Pits, one of the world's richest and most important Ice Age fossil localities, is particularly celebrated for its extinct large mammal fauna, which included species such as sabertooth cats (Smilodon), dire wolves (Canis dirus), and mammoths (Mammuthus). But this locality is also prized for yielding other kinds of fossils, asphaltimpregnated invertebrates, and plants. Such three-dimensional fossils may exhibit structural details that provide a means for securely identifying species that have not been studied as much in depth as the so-called “trophy” fossils from Rancho La Brea (Stock and Harris, 1992). The collection of thirteen galls identified in this study not only show the potential for acquiring novel paleoecological information from still-unstudied insects and plants from this locality but also augments the paltry fossil gall record for all gall inducers and for fossils that should be reported in greater abundance (Larew, 1986, 1987, 1992). Plants increase the production of hormones to create galls or abnormal growths in response to chemical and/or mechanical stimulation ⁎ Corresponding author at: Richard Gilder Graduate School at the American Museum of Natural History, 79th at Central Park West, New York City, New York 10024, USA. E-mail addresses: [email protected] (A.R. Holden), [email protected] (D.M. Erwin), [email protected] (K.N. Schick), [email protected] (J. Gross).
from invaders such as bacteria, fungi, mites, and insects (Mani, 1992; Labandeira, 2002; Russo, 2006). Cynipine wasps oviposit into selective, growing plant tissue. Once larvae hatch, secretions from their feeding cause the acceleration of production of plant tissue, which serves as food and shelter. In effect, the walls of the larval chamber are a nutritious layer of cells or a nutrient sink that renews as the larvae grow and feed (Dreger-Jaufret et al., 1992; Labandeira, 2002; Stone and Schönrogge, 2003, Stone and Schönrogge, 2003; Shorthouse et al., 2005; Russo, 2006). Other specialized cells on the outer layer of the gall can include tannins and starch, which may repel enemies (Dreger-Jaufret and Shorthouse, 1992; Russo, 2006). Among gall insects, cynipines form the most structurally complex and varied galls, including both unilocular (single-chambered) and multilocular (multi-chambered) types that are often diagnostic at the species level (Rohfritsch, 1992; Stone and Schönrogge, 2003; Csóka et al., 2005; Russo, 2006; Bailey et al., 2009). The oak gall wasps (Hymenoptera: Cynipidae: Cynipini) comprise over 940 species worldwide and are only surpassed by gall midges (Diptera: Cecidomyiidae) as the most common gall insect (Felt, 1940; Dreger-Jaufret and Shorthouse, 1992). According to Roskam (1992), Cynipini arose 25 million years ago in the Miocene. However, Rasnitsyn and Quicke (2002) assign their putative age to the Late Cretaceous. The fossil-calibrated divergence estimate of Buffington et al.
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Please cite this article as: Holden, A.R., et al., Late Pleistocene galls from the La Brea Tar Pits and their implications for cynipine wasp and native plant distribution in souther..., Quaternary Research (2015), http://dx.doi.org/10.1016/j.yqres.2015.09.008
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(2012) suggest Cynipini arose approximately 50 million years ago, and the deeper split between the phytophagous cynipids and entomophagous figitids is dated to approximately 125 million years ago, give or take 25 million years. Most gall wasps within Cynipini are associated with Quercus spp.; their distribution and diversity concurs with that of oaks, regarded as the dominant tree species in temperate, deciduous forests in the Northern Hemisphere at the beginning of the early Paleogene (Roskam, 1992). A much smaller proportion of cynipid species, in tribes other than Cynipini, are associated with dicotelydonous angiosperms, while others are inquilines in galls induced by other species (Roskam, 1992; Ronquist, 1999). Larew (1987, 1992) compiled the fossil record of cynipine oak galls, which has also been reviewed by Waggoner and Poteet (1996), Waggoner (1999), Erwin and Schick (2007) and recently by Knor et al. (2013). The first galls definitely attributed to cynipines are at least 20 million years old (Straus, 1977; Scott et al, 1994; Dieguez et al., 1996; Waggoner and Poteet, 1996; Waggoner, 1999). Larew (1986, 1987, 1992) noted that one of the weaknesses in the fossil record of galls is a general incompleteness and unexplained lack of material from the Quaternary (1992). Recent publications have begun to fill in those gaps for cynipine oak galls (Erwin and Schick, 2007) and include additional records for the Quaternary (Stone et al., 2008; Knor et al., 2013). Only two galls from Rancho La Brea have been previously reported. Larew (1987) described the acorn galls of Callirhytis milleri Weld (= C. flora Weld), a species that galls the acorns and petioles of Quercus agrifolia Née, Q. wislizenii A.DC, and Q. kellogii Newb. (all black oaks) (Weld, 1957). Callirhytis milleri is now known to be the alternate bisexual generation of C. flora Weld, a species that galls the petioles of Q. agrifolia, Q. wislizeni, and Q. kelloggii (Weld, 1957). This is a scarce record of fossil cynipine galls considering that three species of oak, Quercus dumosa Nutt., Q. lobata Née, and Q. agrifolia, have been identified from the tar pits (Templeton, 1964; Stock and Harris, 1992) and are known to host more gall-inducing organisms than any other plant, including dozens of cynipine species (Dreger-Jaufret and Shorthouse, 1992; Russo, 2006). However, Larew (1992) noted that many galls have probably remained unnoticed in paleobotany collections, no doubt because of their morphological similarities to certain plant organs. Thus, we first began our focused effort to locate galls by examining curated fruits and seeds in the George C. Page Museum botany collection. Subsequently, we studied unidentified bulk plant material from past and recent excavations. Most of the specimens we identified are virtually intact, although some have suffered slight surface abrasion and/or change in color due to asphalt saturation. A few galls were partial or fragmented. Only two species of insects identified from Rancho La Brea are considered to be extinct (scarab beetles that likely specialized on the dung of extinct mammals); all other recovered species are said to be identical to or conspecific with extant taxa (Miller et al., 1981; Miller, 1983; Stock and Harris, 1992). More generally, many researchers have observed that virtually all Quaternary insects are identical to modern species, which has stimulated a resurgent interest in their systematics and use as paleoenvironmental indicators (Miller, 1983; Elias, 1994; Coope, 2004). In light of this and evidence that cynipines have conserved plant hosts over the last 20 million years (Stone et al., 2009), our procedure was to identify fossils using modern gall morphology. Materials and methods Specimens from Pits A and 3 were excavated between 1913 and 1929. These pits are separate asphaltic deposits located in Hancock Park, a mid-city region within Los Angeles, California; fossil material was cleaned with kerosene and xylol to remove asphalt and substrate, resulting in individually separated specimens with clearly visible detail. Specimens from Pit 3 were found within the skull cavity of a sabertooth cat. The rest of the material studied was excavated from Boxes 1, 5B, 11,
and 14, which represent different asphaltic deposits from Project 23, an ongoing excavation of 16 asphaltic fossiliferous deposits along the western edge of the La Brea Tar Pits. The deposits were exposed, crated into 23 wooden boxes, and transported to a nearby compound for examination. Apart from specimens from 5B, found compacted inside a Camelops hesternus Leidy skull, all identified gall fossils were located in bulk matrix surrounding bones. The fossils were carefully extracted, soaked in Gentech N-propyl bromide to dissolve asphalt, then rinsed with water, resulting in completely separated specimens. Specimens from Rancho La Brea, California Academy of Sciences, and the Essig Museum of Entomology at the University of California, Berkeley were photographed with a Canon EOS 7D digital camera using MP-E 65 mm or 100 mm macro lenses with an attached MT-24EX Macro Twin Lite flash. Specimens from the American Museum of Natural History were photographed with a Visionary Digital photomicrographic apparatus with Infinity optics and Canon EOS 7D. All of the above images were processed using Adobe Photoshop CS6 Extended. Some of the material was radiographed using a Faxitron cabinet x-ray, model 43855C, printed on Kodak M125 Industrex film, and developed in a darkroom using photographic chemicals to determine the location and orientation of larval chambers. The radiographs were placed on a light box and photographed with a Cannon EOS Rebel XSi 450D with an EF-260 mm f/2.8 Macro USM lens. Images were processed with Adobe Photoshop CS5 to allow for higher-resolution examination. Integral stem galls with similar external morphology were CT scanned to aid in identification of fossil material by analyzing location and orientation of larval chambers, which were then compared to radiographs of fossil material. Scanning was performed on a GE Phoenix vtomex s 240 at 60 kV and 180 μA for 5-second exposures. Resulting images were 4 × 4 μm per pixel in resolution, stitched together in Image J v1.45 and rendered in Volume Graphics Studio Max v2.2. All fossil specimens are housed at the George C. Page Museum, a branch of the Natural History Museum of Los Angeles County. Cynipine gall morphology is often species-specific and therefore can be firmly attributed without observation of the insect responsible (Rohfritsch, 1992; Stone and Schönrogge, 2003; Csóka et al., 2005; Russo, 2006; Bailey et al., 2009). Visual comparisons of material, as well as radiographs and CT scans, were made using the L.H. Weld Collection of galls at the California Academy of Sciences in San Francisco, specimens from the Essig Museum of Entomology at the University of California, Berkeley, the American Museum of Natural History, and personal observations (A.R.H., D.M.E, K.N.S, and J.G.) of cynipine galls in the field. Systematic paleontology Order HYMENOPTERA Linnaeus, 1758 Superfamily CYNIPOIDEA Ashmead, 1899 Family CYNIPIDAE Westwood, 1840 Tribe CYNIPINI Ashmead, 1903 Genus DIASTROPHUS Hartig, 1840 cf. Diastrophus niger Bassett, 1900 Material. – LACMHC 475B. Description. – LACMHC 475B is a multilocular, cylindrically shaped, possibly integral stem gall that is 6.4 mm long and 3.7 mm wide. There are no remains of the stem preserved. The gall is composed of at least five larval chambers that are up to 2.5 mm wide, with some chambers showing circular exit holes (Figure 1A–C.). There is very little tissue separating what appear to be relatively simple chambers, a character apparent in modern D. niger galls (Figure 1D–F). Occurrence. – Late Pleistocene. Rancho La Brea Tar Pits, Pit A. Remarks. – This gall is slim, stem-like, with few cells and has a general lumpy external morphology (unlike linear D. fragariae Beutenmuller), as if the petiole layer had worn away. Host. – Cinquefoil (Potentilla). Diastrophus sp.
Please cite this article as: Holden, A.R., et al., Late Pleistocene galls from the La Brea Tar Pits and their implications for cynipine wasp and native plant distribution in souther..., Quaternary Research (2015), http://dx.doi.org/10.1016/j.yqres.2015.09.008
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Fig. 1. Diastrophus niger. A–C) LACMHC 475B. Scale bar equals 1 mm. D, F) Modern material. Scale bar equals 5 mm. E) CT scan cross-section of F. Scale bar equals 2 mm.
Material. – LACMHC 470Ba (Figure 2A–C), 470Bb (Figure 2A), LACMP23 11092 (Figure 2D–F). Description. – LACMHC 470Ba and b are parts of a single multilocular stem gall. There is very little tissue between the larval chambers, which are held together by thin sheaths of tissue. LACMHC 470Bb is tapered at one end and widens toward the other (viz.) teardrop shaped. The complete gall is 8.0 mm long and 5.0 mm wide, and shows the possible remnant of a slender stem at the narrow end of the gall (Figure 2B, C). There are about seven chambers, which are each about 3 mm in their longest dimension. In places where the chamber walls are broken, these walls are notably thin. The chambers abut one another and their shapes vary. LACMP23 11092 is another fragment of a multilocular gall similar to LACMHC 470Ba and b (Figure 2D–F). This specimen is 6.0 mm long and 3.4 mm wide. It has six to seven chambers that are 2.0–2.5 mm wide, and there are two exit holes (Figure 2D).
Occurrence. – Late Pleistocene. Rancho La Brea Tar Pits. LACMHC 470Ba and 470Bb are from Pit A; LACMP23 11092 is from Project 23, Box 5B. Remarks. – Diastrophus is distinguished from other cynipid galls by simplest structure and little tissue specialization. Host. – Rosaceous hosts such as Cinquefoil (Potentilla), brambles (Rubus), and wild strawberry (Fragaria). Genus NEUROTERUS Hartig, 1840 cf. Neuroterus cupulae Kinsey, 1922 Material. – LACMP23 11112 (Figure 3A, B). Description. – LACMP23 11112 is the remains of a small, partial acorn cap (involucre), 4.6 mm wide and 2.2 mm high, covered with tiny, overlapping triangular scales, 0.7 mm wide near their base and 0.8 mm long (Fig. 3A, B). This specimen shows two circular holes (Figure 3 A, B). The interior hole is 0.7 mm wide (Figure 3B) and the other smaller exterior hole is 0.5–06 mm wide (Figure 3A). The exterior hole represents an exit
Fig. 2. Diastrophus sp. A) 470Ba, 470Bb. B, C) LACMHC 470Ba. D-F) LACMP23 11092.
Please cite this article as: Holden, A.R., et al., Late Pleistocene galls from the La Brea Tar Pits and their implications for cynipine wasp and native plant distribution in souther..., Quaternary Research (2015), http://dx.doi.org/10.1016/j.yqres.2015.09.008
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Fig. 3. Neuroterus cupulae. A, B) LACMP23 11112, with exit hole and (B) with larval chamber. Scale bar equals 2 mm. C, D) Modern material, with larval chambers and exit holes. Scale bar equals 5 mm.
hole located in the cap. Internal to the external hole and lying below the floor of the nut, there is a cavity that appears to be a former larval chamber (Figure 3B). The relationship of the larger internal hole to the nut or chamber lying below it is not clear. Similar larval chambers and exit holes are visible in modern, comparative material (Figure 3C, D). Occurrence. – Late Pleistocene. Rancho La Brea Tar Pits, Project 23, Box 11. Remarks. – It cannot be entirely ruled out that an acorn-feeding weevil produced the exit hole. Host. – Valley oak (Q. lobata ), (Kinsey and Ayres, 1922), coastal sage scrub oak (Q. dumosa), and blue oak (Q. douglasii Hook. and Arn.). Genus ANDRICUS Hartig, 1840 Andricus occultatus Weld, 1926 Material. – LACMHC 479B. Description. – LACMHC 479B is a tiny bud gall, 2.8 mm long and 1.6 mm wide (Figure 4A). The gall is laterally compressed and consists of a small circular base, 0.8 mm wide, and with over 20 minute imbricate scales, the basal ones measuring about 1.0 mm, decreasing in size apically (Figure 4A). There is a well-defined exit hole, about 0.4 mm
Fig. 4. Andricus occulatus. A) LACMHC 479B, with exit hole. Scale bar equals 1 mm. B) Modern material, with exit hole. Scale bar equals 1mm.
wide, located in the mid-region on the flattened side of the gall (Figure 4A). Occurrence. – Late Pleistocene. Rancho La Brea Tar Pits, Pit A. Remarks. – LACMHC 479B is virtually indistinguishable from modern material; the size and morphology of the bud and exit hole are the same as extant examples of this species (Figure 4B). Host. –White oaks, which include valley oak (Q. lobata), leather oak (Q. durata Jep.), Nuttall's scrub oak (Q. dumosa), scrub oak (Q. berberidifolia Liebm.), blue oak (Q. douglasii), and Oregon oak (Q. garryana Doug. ex Hook.). Genus BESBICUS Kinsey, 1930 cf. Besbicus conspicuus Kinsey, 1930 Material. – LACMP23 11106. Description. – The specimen has a smooth, strongly rugose surface pattern (Figure 5A, B). It is 6.6 mm at its widest diameter, and the shortest is 5.8 mm (Figure 5A, B). The radiograph (Figure 5C) shows a single, central chamber surrounded by tissue. Occurrence. – Late Pleistocene. Rancho La Brea Tar Pits, Project 23, Box 11. Remarks. – Similar to the unilocular galls of Besbicus conspicuous (Figure 5C, D). This species is mislabeled as Disholcaspis washingtonensis Gillette in Russo (2006). Host. – Pacific white oaks, which include blue oak (Q. douglasii), deer oak (Q. sadleriana Brown), Engelmann oak (Q. engelmannii Greene), leather oak (Q. durata), Nuttall's scrub oak (Q. dumosa), scrub oak (Q. berberidifolia), and valley oak (Q. lobata) (Russo, 2006). Genus DISCHOLCASPIS Dalla Torre and Kieffer, 1910 cf. Disholcaspis prehensa Weld, 1957 Material. – LACMHC 477B (Figure 6A–C) and LACMP23 13422 (Figure D–F). Description. – Both specimens are reminiscent of the multilocular stem galls of Disholcaspis prehensa. LACMHC 477B has a flared base 7.0 mm wide and the gall is 6.5 mm tall (Figure 6A–C). The apical cap area is circular, 4.0 mm wide and 0.8 mm thick (Figure 6A–C). A rim (carina) encircles the base of the cap where it attaches to the main body of the gall (Figure 6A–C). The cap surface is rugose and divided into small wedges (Figure 6B). The tissue of the main gall body has a rough, degraded texture (Figure 6A–C). LACMP23 13422 is approximately 6.0 mm wide and has an ovoid rugose cap, 2.3 mm wide and 0.7 mm thick (Figure 6D–E). Portions of the sides of the main gall body are flaking off; the outer layer is thin and appears to have separated from the inner spongy tissue of the gall wall (Figure 6D). Occurrence. – Late Pleistocene. Rancho La Brea Tar Pits. LACMHC 477B is from Pit A; LACMP23 13422 is from Project 23, Box 1. Remarks. – While portions of the specimens have exfoliated, enough remains to discern their resemblance to D. prehensa (Figure 6F). Host. – Pacific white oaks, which include blue oak (Q. douglasii), deer oak (Q. sadleriana), Engelmann oak (Q. engelmannii), leather oak (Q. durata), Nuttall's scrub oak (Q. dumosa), scrub oak (Q. berberidifolia), and valley oak (Q. lobata) (Russo, 2006). Genus DRYOCOSMUS Giraud, 1859 cf. Dryocosmus dubiosus Material. – LACMP23 12854. Description. – This specimen (Figure 7A–D) resembles the unilocular leaf galls of D. dubiosus (Figure 7E, F). The specimen is boat-shaped and measures 3 mm long and 1.5 mm wide. There is a minute circular hole, 0.10 mm wide, located on the underside of the specimen; this may be an exit hole (Figure 7C, D). Occurrence. – Late Pleistocene. Rancho La Brea Tar Pits, Project 23, Box 1. Remarks. – Similar to the extant gall (Figure 7 E, F) but also resembles Arctostaphylos seeds and hole may be predation. Host. – Black oaks including California black oak (Q. kellogii), coast live oak (Q. agrifolia), and interior live oak (Q. wislizenii ) (Russo, 2006). Genus CALLIRHYTIS Förster, 1869
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Fig. 5. Besbicus conspicuus. A–C) LACMP23 11106. C) Radiograph of LACMP23 11106. Scale bar equals 2 mm. D, E) Modern material, whole and cross-sectioned. Scale bar equals 2 mm.
c.f. Callirhytis quercussuttoni (Basset) Dalla Torre and Kieffer, 1910 Andricus quercussuttoni (Dalla Torre and Keiffer) Melika and Abrahamson, 2002) Material. – LACMHC 430B (Figure 8A–C) and LACMHC 431Bb (Figure 8D–F). Description. – LACMHC 430B is a multilocular integral stem gall resembling the extant galls of Callirhytis quercussuttoni (Figure 8A-H). It is ovoid in shape, 1.5 cm long by 1.0 cm wide, with the stem visibly running through the gall and portions of it sticking out at each end (Figure 8A–C). The gall is somewhat asymmetrical in being flattened on one side with the stem not running through the center of the gall (Figure 8B). No larval chambers are visible on the flattened side the gall (Figure 8B). Four exit holes, approximately 0.8 mm diameter, with distinctive rims are visible and correspond to the underlying larval chambers (Figure 8A). Though not exceptionally clear, the radiograph does appear to show the chambers are separated by tissue (Figure 8C). CT scans (Figure 8G) also show chambers separated by tissue but sometimes closely abutting. LACMHC 431Bb is a multilocular, integral stem gall (Figure 8D–F). It is ovoid measuring 2.1 cm long and 1.5 cm wide, with a short remnant of its narrow 3.0 mm wide branch, still attached (Figure 8D, E). On one side of the specimen, a couple of pieces have broken off exposing the interior of the gall revealing the larval chambers (Figure 8D, E). Larval chambers are 2.0–2.5 mm wide with openings that may be exit holes. This gall is pear-shaped and slightly beaked (Figure 8D, E). There are at least 15 chambers visible in the exposed area. On the unbroken surface, there is evidence of larval chamber position and exit holes, which are infilled with asphalt (Figure 8D). In surface view, there appears to be tissue between the chambers, but the radiograph shows there is very little tissue separating the chambers (Figure 8E). The chambers are numerous, closely spaced, and the inclosing cavities somewhat angular in section view (Figure 8E). Occurrence. – Late Pleistocene. Rancho La Brea Tar Pits, Pit A. Remarks. – Diagnostic to species-level features include tissue in between cells (Figure 8C–G), exit holes on outside (Figure 8A, H), rim around exit holes (Figure 8A, H), stem tissue in between (Figure 8A, B, D, E), cells oriented around stem (Figure 8C), cells oriented in the same direction (Figure 8F). Russo (2006) describes these galls as
forming abruptly on the stems, suggesting there is little taper where the gall and stem meet. Though many C. quercussuttoni galls do show little taper at the gall-stem junction, some are more tapered. In A. spectabilis Kinsey or Dryocosmus asymmetricus Kinsey the stems are typically more tapered at the gall-stem juncture. However, some C. quercussuttoni galls do have stems that taper at the gall-stem juncture. LACMHC 431Bb also shows some similarity to A. spectabilis, which has external exit holes, chambers oriented toward gall surface so exit holes directly face outward, and there is tissue between the chambers. However, there is also some similarity to modern D. asymmetricus, which shows very little tissue separating larval chambers. Host. – Black oaks, which include California black oak (Q. kellogii), coast live oak (Q. agrifolia), and interior live oak (Q. wislizenii) (Russo, 2006). cf. Callirhytis quercuspomiformis Bassett, 1881 (Amphibolips quercuspomiformis (Bassett) Melika and Abrahamson, 2002) Material. – LACMHC 431Ba. Description. – This specimen is a woody, multilocular detachable stem gall (Figure 9A–C). It is asymmetrically shaped, rounded on one side and flattened on the other (Figure 9A–C). It measures 13.4 mm long, 9.9 mm tall and 10.5 mm wide, and contains at least 20 chambers, with roughly circular outlines (Figure 9A–C). The chambers are oriented perpendicular to the long axis of the gall, arranged in a regular pattern, and with tissue in between (Figure 9A– C).) Chambers are relatively large and of various sizes as seen in different levels of section and views (Figure 9A–C). They measure 1.8–2.8 mm wide and up to 4.5 mm long (Figure 9A–C). The specimen appears to be worn and abraded, with the inner layers of the chambers no longer preserved and filled in with asphalt (Figure 9A–C). Occurrence. – Late Pleistocene Rancho La Brea Tar Pits, Pit A. Remarks. – This specimen most closely resembles the detachable stem galls of Callirhytis quercuspomiformis (Figure 9D, E. There are morphological similarities and differences to Diastrophus kincaidii Gillette, a multilocular integral stem gall found on thimbleberry (Rubus parviflorus Nutt.) such as the globular shape and radial orientation of larval cells around the stem (Russo, 2006; Weld, 1957).
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Fig. 6. Disholcaspis prehensa. A–C) LACMHC 477B, carina visible. Scale bar equals 1 mm. D, E) LACMP23 13422, carina visible, layers, other layers flaking off. Scale bar equals 1 mm. F) Modern material, approximately 10 mm wide at the base with caps about 5 mm wide.; 7–10 mm high (Russo, 2006).
Host. – Black oaks, which include California black oak (Q. kellogii), coast live oak (Q. agrifolia), and interior live oak (Q. wislizenii) (Russo, 2006). cf. UNDESCRIBED EXTANT GALL Material. – LACMHC 468B. Description – This specimen has a circular hole, most likely an exit hole, 0.4 mm wide, located on the side of the gall (Figure 10A). There is a raised knob, 0.5 mm long, 0.4 mm wide, and 0.1 mm thick on the lower surface of LACMHC 468B (Figure 10A–C). It has an ovoid shape with a somewhat irregular outline (Figure 10A–C). The area of the gall wall near the knob has fine linear striations radiating out from the base of the knob (Figure 10C). Surface of the knob appears pitted (Figure 10A–C). The surface of the main body is characterized by minute tubercles scattered over the gall surface (Figure 10A–C). Occurrence. – Late Pleistocene Rancho La Brea Tar Pits, Pit 3. Remarks. – This gall resembles extant, undescribed galls of similar size, shape, and surface structure that occur on the leaves of canyon live oak (Q. chrysolepis Liebm.) (Figure 10D–H). Host. – Possibly canyon live oak (Q. chrysolepis).
Discussion The collection of Rancho La Brea galls described here represents new records for the late Pleistocene of western North America for Callirhytis, Diastrophus, Disholcaspis, Andricus, Neuroterus, Besbicus, and Dryocosmus, as well as providing minimum probable dates and revealing an undescribed species. It also contributes to the Cenozoic fossil record of galls, especially for the Quaternary, for which few identified specimens are known (Larew, 1992). Three-dimensional fossil galls are extremely rare (Larew, 1986, 1992; Stone et al., 2008). The vast majority of galls in the fossil record are preserved as compressions, which often lack the structural complexity necessary to identify the gall maker, as well as potential host plants, parasites, and inquilines (Stone et al., 2008). Recognizing fossil galls can be a challenge and many have been mistaken for typical plant parts like cones, inflorescences, fruits, and seeds. Many nondescript holes on fossil leaves have been attributed to gallers and interpreted as sites of former gall attachments. However, discerning this type of damage from similar types caused by bacteria, fungi, leaf
Please cite this article as: Holden, A.R., et al., Late Pleistocene galls from the La Brea Tar Pits and their implications for cynipine wasp and native plant distribution in souther..., Quaternary Research (2015), http://dx.doi.org/10.1016/j.yqres.2015.09.008
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Fig. 7. Dryocosmos dubiosus, asexual, fall generation. A–D) LACMP23 12854. Scale bar equals 1 mm. C, D) Probable exit hole. E, F) Modern material of the asexual gall, variable, but similar in length.
damage due to puncturing, or other physical non-biological causes, or the feeding of phytophagous insects, is difficult. In contrast, the unique fossil preservation at the La Brea Tar Pits provides an opportunity to study three-dimensionally intact and original material, thus lending high confidence to identifications. Larew (1992) noted that many fully interpretable fossil galls may be left unnoticed in museum collections. Rancho La Brea's holdings are a good example: although a few have been recognized, prepared, and curated, this paper demonstrates that many more can be identified and described in considerable detail, given the great abundance of oak and other major gall hosts recovered there. One of the more significant aspects of this fossil gall collection is that it indicates the late Pleistocene presence of host plants that have not yet been recognized as such at Rancho La Brea based on our hypothesis of extant gall species specificity. Potential, but unrecorded, hosts include oak species such as Pacific white oak species—Blue oak (Q. douglasii), deer oak (Q. sadleriana), Engelmann oak (Q. engelmannii), leather oak (Q. durata), and scrub oak (Q. berberidifolia)—Black oaks including California black oak (Q. kellogii) and interior live oak (Q. wislizenii)—as well as Cinquefoil (Potentilla), and wild strawberry (Fragaria). The presence of these hosts offers clues to the local paleo14 environment between approximately ~2200 and 60,000 C yr BP, but with most specimens provisional dated to between ~ 30,000 and 14 48,000 C yr BP. While the La Brea galls have not been directly dated, ranges of dates on other material from these deposits have been acquired at the W. M. Keck Carbon Cycle Accelerator Mass Spectrometry Laboratory at University of California, Irvine (Fuller et al., 2014). Specific
14
intervals dated thus far include Pit A, which is ~2200 to 47,000 C yr BP; 14 Pit 3, which is ~14,000–21,000; C yr BP; Project 23 Box 1, which is from 14 ~30,000 C yr BP to older than can be measured with radiocarbon dat14 ing, but with a high proportion of dates between 35,000 and 37,000 C 14 yr BP; 5B, which is ~42,000–47,000 C yr BP; Box 11, which has one date 14 at 37,000 C yr BP; and the range for Box 14 , which is ~42,000–48,000 14 C yr BP (Fuller et al., 2014; J.R. Southon, pers. comm.). All of the Rancho La Brea gall-forming cynipines are evidently extant. Each indicates the presence of a host plant with known, modern current climatic range. Thus these fossil data could provide new insights concerning late Ice Age environmental conditions prevailing in southern California. However, there are caveats. The host plants identified on the basis of fossil galls occur in a diverse range of habitats in present-day California. These environments include coniferous forest, mixed evergreen, woodlands–savannah, and chaparral (Munz and Keck, 1959; Ordnuff et al., 2003; Baldwin et al., 2012). Among these habitats, the average precipitation currently ranges from as little as approximately 35 to as much as 280 cm per year (Munz and Keck, 1959; Ordnuff et al., 2003); the average winter minimum is as low as − 1.6°C and the average summer maximum is as high as 35°C (Munz and Keck, 1959; Ordnuff et al., 2003); and host plants presently occur in elevations ranging from approximately 45–760 m (Baldwin et al., 2012). Given such an implausibly large range of ecological conditions during a narrow time interval at Rancho La Brea, supported by the aforementioned, wide provisional date ranges for the galls, the only plausible conclusion is that some gall specimens found there in fact originated elsewhere, and were secondarily deposited by fluviatile conditions and alluvial wash (Shaw and Quinn,
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Fig. 8. Callirhytis quercussuttoni. A–C) LACMHC 430B. Scale bar equals 5 mm. A) Exit holes surrounded by round, flat rim. A, B, D, E) Stem visible. C) Radiograph shows chambers separated by tissue. D–F) LACMHC 431Bb. Scale bar equals 5 mm. D) Chamber separated by tissue. D–E) Exposed chambers, branch visibly attached. F) Radiograph shows little tissue separating chambers. G) CT scan cross-section of H (modern material). Both with scale bar equal to 5 mm. H) Exit holes with flat rims.
1986). Possibly, the abraded specimens represent transportation from such nonlocal habitats, although abrasion could also occur in the case of asphaltic movement within tar pits, whereas the more intact specimens were dropped in situ at Rancho La Brea.
Although the fossil gall collection described in this paper is of limited value for interpreting paleocological conditions in the immediate environs of Rancho La Brea, it has much significance nevertheless. Assuming that ecological conditions required by native plants in California during
Fig. 9. Callirhytis quercuspomiformis, asexual, summer generation. A–C) LACMHC 431Ba, chambers oriented perpendicular to long axis of the gall, arranged in regular pattern, and with tissue in between. Scale bar equals 5 mm. D, E) Modern material, with similar chamber orientation around stem. Scale bar equals 1 cm.
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Fig. 10. Undescribed gall. A–C) Exit hole, bottom knob, and adjacent striations. Scale bar equals 0.5 mm. D–H) Similar surface structure, shape, knob. Scale bar equals 0.5 mm.
the late Pleistocene were the same as those prevailing today, the taxonomic diversity of the fossil galls indicates that almost every habitat in the state today existed during the late Pleistocene. Does this, in turn, imply that regional plant communities have not drastically changed since the late Pleistocene? This has been suggested by some studies on Rancho La Brea plant fossils (Templeton, 1964; Warter, 1976). Currently, Rancho La Brea plant fossils have been used to reconstruct four plant associations: chaparral, coastal sage scrub, deep canyon, and riparian (Shaw and Quinn, 1986; Stock and Harris, 1992). While many of the fossil gall hosts fit within these groups, new host records, including Quercus kellogii, sadleriana, wislizenii, and garrayana, as well as Rubus parviflorus, are consistent with the kinds of mesic ecological conditions found at elevations higher than those preferred by the current coastal sage scrub community (Holden et al., 2014). By the same token, the occurrence of gall-forming insects that thrive in hot and even arid conditions (Holden et al., 2013) is also discordant with conditions prevailing at Rancho La Brea today. Clearly, original provenance and age are all-important: only when the content of the local fossil entomofauna is firmly established for Rancho La Brea, in sufficient abundance to permit destructive sampling, will a clear understanding of ecological change and continuity at Rancho La Brea emerge (Shaw and Quinn, 1986; Holden et al., 2014). In closing, we emphasize that La Brea cynipine galls are fossils of substantial but undervalued significance. Not only do they permit identification of hosts otherwise unknown, they may also provide evidence for the occurrence of other fossils of great interest, such as potential inquilines, parasites, parasitoids, predators, and even fungi that form the micro-communities of complex galls (Mani, 1992; Csóka et al., 2005; Stone et al., 2008). Rancho La Brea's lesser known yet immense insect and plant collections are a storehouse of data for reconstructing regional late Pleistocene climate, habitats, flora, and vegetation—when dated, these insect communities can potentially provide a high-resolution snapshot of the prehistoric paleoenviroment of the Rancho La Brea Tar Pits and the conditions that provided food, shelter, and other necessities of life for the doubtlessly charismatic, but nonetheless utterly dependent, megafauna.
Acknowledgments We thank the following individuals: From the American Museum of Natural History—J. Carpenter and R. MacPhee provided review, and C. Lebeau provided access to comparative material; S. Tucker provided many photographic images; M. Hill, H. Towbin, and P. Barden coordinated and assisted in CT scanning; funding from the Museum supported this project. George C. Page Museum—J. Harris offered financial support; S. Cox, A. Farrell, G. Takeuchi, and T. Valle expedited the preparation and documentation of specimens for the study and provided information on specimen excavation and provenance; C. Howard provided many photographic images for research and publication; L. Tewksbury, C. Howard, M. Tabencki, K. Rice, and C. Lutz were involved in Project 23 excavation. From the Natural History Museum of Los Angeles County—L. Chiappe provided review and guidance, and R. Hulser assisted with references; funding from the Museum supported this project. From the University of California, Irvine— J. Southon, B. Fuller, and S. Fahrni provided dates of specimens within Project 23 deposits. From the United States Department of Agriculture—M. Buffington provided extensive review. We also thank G. Csóka, S. Elias, B. R. Barton, and A. Gillespie for their constructive review. References Bailey, R., Schönrogge, K., Cook, J.M., Melika, G., Csóka, G., Thuróczy, C., Stone, G.N., 2009. Host niches and defensive extended phenotypes structure parasitoid wasp communities. PLoS Biol. 7 (8), e1000179. Baldwin, B.G., Goldman, D.H., Keil, D.J., Patterson, R., Thomas, J.R., 2012. The Jepson Manual. Vascular plants of California, Second edition University of California Press, Berkeley, Los Angeles, and London. Buffington, M.L., Brady, S.G., Morita, S.I., Van Noort, S., 2012. Divergence estimates and early evolutionary history of Figitidae (Hymenoptera: Cynipoidea). Syst. Entomol. 37 (2), 287–304. Coope, G.R., 2004. Several millions of year of stability among insect species because of, or in spite of, Ice Age climatic instability? Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 359, 209–214. Csóka, G., Stone, G.N., Melika, G., 2005. Biology, ecology and evolution of gall-inducing Cynipidae. In: Raman, A., Schaefer, C.W., Withers, T.M. (Eds.), Biology, Ecology and Evolution of Gall-Inducing Arthropods. Science Publishers, Enfield, pp. 573–642. Dieguez, C., Nieves-Aldrey, J.L., Barron, E., 1996. Fossil gall (zoocecids) from the Upper Miocene of La Cerdana (Lerida, Spain). Rev. Palaeobot. Palynol. 94, 329–343.
Please cite this article as: Holden, A.R., et al., Late Pleistocene galls from the La Brea Tar Pits and their implications for cynipine wasp and native plant distribution in souther..., Quaternary Research (2015), http://dx.doi.org/10.1016/j.yqres.2015.09.008
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A.R. Holden et al. / Quaternary Research xxx (2015) xxx–xxx
Dreger-Jaufret, F., Shorthouse, J.D., 1992. Diversity of gall inducing insects and their galls. In: Shorthouse, J.D., Rohfritsch, O. (Eds.), The Biology of Insect-Induced Galls. Oxford University Press, New York, Oxford, pp. 8–33. Elias, S.A., 1994. Quaternary Insects and Their Environments. Smithsonian Institution Press, Washington D.C. Erwin, D.M., Schick, K.N., 2007. New Miocene oak galls (Cynipini) and their bearing on the history of cynipid wasps in western North America. J. Paleontol. 81 (3), 568–580. Felt, E.P., 1940. Plant Galls and Gall Makers. Comstock Publishing Company, Ithaca, New York. Fuller, B.T., Fahrni, S.M., Harris, J.M., Farrell, A.B., Coltrain, J.B., Gerhart, L.M., Ward, J.K., Taylor, R.E., Southon, J.R., 2014. Ultrafiltration for asphalt removal from bone collagen for radiocarbon dating and isotopic analysis of Pleistocene fauna at the tar pits of Rancho La Brea, Los Angeles, California. Quat. Geochronol. 22, 85–98. Holden, A.R., Harris, J.M., Timm, R.M., 2013. Paleoecological and taphonomic implications of insect-damaged Pleistocene vertebrate remains from Rancho La Brea, southern California. PloS One 8 (7), e67119. Holden, A.R., Koch, J.B., Griswold, T., Erwin, D.M., Hall, J., 2014. Leafcutter bee nests and pupae from the Rancho La Brea Tar Pits of southern California: Implications for understanding the paleoenvironment of the Late Pleistocene. PloS One I (4), e94724. Kinsey, A.C., Ayres, K.D., 1922. Studies of Some New and Described Cynipidae (Hymenoptera). University of Indiana, Bloomington. Knor, S., Skuhrava, M., Wappler, T., Prokop, J., 2013. Galls and gall makers on plant leaves from the lower Miocene (Burdigalian) of the Czeck Republic: systematic and paleoecological implications. Rev. Palaeobot. Palynol. 188, 38–51. Labandeira, C.C., 2002. The history of associations between plants and animals. In: Herrera, C.M., Olle, P. (Eds.), Plant-Animal Interactions: An Evolutionary Approach. John Wiley and Sons, Hoboken, New Jersey, pp. 26–76. Larew, H.G., 1986. The fossil gall record: a brief summary. Proc. Entomol. Soc. Wash. 88, 385–388. Larew, H.G., 1987. Two cynipid wasp acorn galls preserved at the La Brea Tar Pits (early Holocene). Proc. Entomol. Soc. Wash. 89 (4), 831–833. Larew, H.G., 1992. Fossil galls. In: Shorthouse, J.D., Rohfritsch, O. (Eds.), The Biology of Insect-Induced Galls. Oxford University Press, New York, Oxford, pp. 50–59. Mani, M.S., 1992. Introduction to cecidology. In: Shorthouse, J.D., Rohfritsch, O. (Eds.), The Biology of Insect-Induced Galls. Oxford University Press, New York, Oxford, pp. 3–7. Miller, S.E., 1983. Late Quaternary insects of Rancho La Brea and McKittrick, California. Quat. Res. 20 (1), 90–104. Miller, S.E., Gordon, R.D., Howden, H.F., 1981. Reevaluation of Pleistocene scarab beetles from Rancho La Brea, California (Coleoptera: Scarabaeidae). Proc. Entomol. Soc. Wash. 83, 625–630. Munz, P.A., Keck, D.D., 1959. A California Flora. University of California Press, Berkeley and Los Angeles.
Ordnuff, R., Fabert, P.M., Wolf, T.K., 2003. Introduction to California Plant Life. University of California Press, Berkeley. Rasnitsyn, A.P., Quicke, D.L. (Eds.), 2002. History of Insects. Kluwer Academic Publishers, Norwell, Massachusetts. Rohfritsch, O., 1992. Patterns in gall development. In: Shorthouse, J.D., Rohfritsch, O. (Eds.), The Biology of Insect-Induced Galls. Oxford University Press, New York, Oxford, pp. 60–86. Ronquist, F., 1999. Phylogeny, classification and evolution of the Cynipoidea. Zool. Scr. 28 (1‐2), 139–164. Roskam, J.C., 1992. Evolution of the gall-inducing guild. In: Shorthouse, J.D., Rohfritsch, O. (Eds.), The Biology of Insect-Induced Galls. Oxford University Press, New York, Oxford, pp. 34–49. Russo, R., 2006. Field Guide to Plant Galls of California and Other Western States. University of California Press, Berkeley and Los Angeles. Scott, A.C., Stephenson, J., Collinson, M.E., 1994. The fossil record of leaves with galls. In: Williams, M.A.J. (Ed.), Plant GallsSystematics Association Special Volume No. 49. Clarenson Press, Oxford, pp. 447–470. Shaw, C.S., Quinn, J.P., 1986. Rancho La Brea: a look at coastal southern California's past. Calif. Geol. 39, 123–133. Shorthouse, J.D., Wool, D., Raman, A., 2005. Gall-inducing insects—nature's most sophisticated herbivores. Basic Appl. Ecol. 6 (5), 407–411. Stock, C.S., Harris, J.M. (Eds.), 1992. Rancho La Brea: A Record of Pleistocene Life in California. Natural History Museum of Los Angeles County, Los Angeles, California. Stone, G.N., Schönrogge, K., 2003. The adaptive significance of insect gall morphology. Trends Ecol. Evol. 18, 512–522. Stone, G.N., van der Ham, R.W.J.M., Brewer, J.G., 2008. Fossil oaks preserve ancient multitrophic interactions. Proc. R. Soc. Lond. B Biol. Sci. 275, 2213–2219. Stone, G.N., Hernandez‐Lopez, A., Nicholls, J.A., Di Pierro, E., Pujade‐Villar, J., Melika, G., Cook, J.M., 2009. Extreme host plant conservatism during at least 20 million years of host plant pursuit by oak gallwasps. Evolution 63 (4), 854–869. Strauss, A., 1977. Gallen, Minen und andere Fraßspuren in Pliozän von Willershausen am Harz. Verhandlungen der Botanischen Vereins der Provinz Badenburg 113, 43–80. Templeton, B.C. 1964. The fruits and seeds of the Rancho La Brea Pleistocene deposits: Oregon State University, Unpublished PhD dissertation. Waggoner, B.M., 1999. Fossil oak leaf galls from stinking water paleoflora of Oregon (middle Miocene). PaleoBios 19 (3), 8–14. Waggoner, B.M., Poteet, M.F., 1996. Unusual oak leaf galls from the middle Miocene of northwestern Nevada. J. Paleontol. 70, 1080–1084. Warter, J.K., 1976. Late Pleistocene plant communities—evidence from the Rancho La Brea Tar Pits. Symposium proceedings on plant communities of southern California. Calif. Native Plant Soc. Spec. Pub. volume 2, pp. 32–39. Weld, L.H., 1957. Cynipid galls of the Pacific slope. Privately Printed.
Please cite this article as: Holden, A.R., et al., Late Pleistocene galls from the La Brea Tar Pits and their implications for cynipine wasp and native plant distribution in souther..., Quaternary Research (2015), http://dx.doi.org/10.1016/j.yqres.2015.09.008