PUBLISHED BY THE AMERICAN MUSEUM OF NATURAL HISTORY CENTRAL PARK WEST AT 79TH STREET, NEW YORK, NY 10024 Number 3611, 17 pp., 7 figures, 1 table April 9, 2008 An Unusual, Primitive Piesmatidae (Insecta: Heteroptera) in Cretaceous Amber from Myanmar (Burma) DAVID A. GRIMALDI1 AND MICHAEL S. ENGEL2 ABSTRACT Cretopiesmasuukyiae,newgenusandspecies,isdescribed,basedonauniquefemalespecimenin mid-Cretaceous(c.100myo)amberfromnorthernMyanmar.FeaturesofC.suukyiaeuniquefor the small Recent family Piesmatidae include a long, protrudent clypeus, a dorsal carina of the head, lack of ‘‘jugal’’ lobes/appendices, widely separated coxae, very large scutellum, and the venation of the corium; some of these are plesiomorphic and shared with Aradidae. C. suukyiae possessesthecuticular areolationandpropleuralcavities distinctivetoPiesmatidae. Phylogenetic analysis of Recent and fossil genera of piesmatids resulted in a cladogram with Cretopiesma as sister group to the remainder of the family. Relationships of this unusual species and of PiesmatidaewithinPentatomomorpha are discussed. INTRODUCTION Tingidae (see the historical reviews by Drake and Davis, 1958; Heiss and Pe´ricart, 1983). The Piesmatidae is a small family of Not until the work of Tullgren (1918), Leston approximately 40 Recent species and three etal.(1954),andDrake andDavis(1958)was genera, which are rather small in size (gener- the position of the family within the Pentato- ally 2–4 mm long) and have extensive areola- momorpha established, though relationships tion of the head, thorax, and corium of the within this infraorder are still obscure. hemelytra. The distinctive microsculpture ini- Piesmatids have been considered to have an tially led hemipterists to classify these bugs isolated position in the Pentatomomorpha within or near the cimicomorphan family (Sˇtys, 1967), to be within the ‘‘malcid line’’ 1DivisionofInvertebrateZoology(Entomology),AmericanMuseumofNaturalHistory([email protected]). 2Division of Invertebrate Zoology (Entomology), American Museum of Natural History; Division of Entomology (Paleoentomology),NaturalHistoryMuseum,andDepartmentofEcology&EvolutionaryBiology,1501CrestlineDrive –Suite140,UniversityofKansas,Lawrence,Kansas66049-2811([email protected]). CopyrightEAmericanMuseumofNaturalHistory2008 ISSN0003-0082 2 AMERICAN MUSEUMNOVITATES NO. 3611 (Malcidae,Colobathristidae,Berytidae)ofthe to feed on three genera of chenopods, an Lygaeoidea (Schaefer, 1972, 1981), or closely amaranth (Amaranthus), and even a sedge related to the rare, coleopteriform lygaeoids, (Cyperaceae). Several species feed on Acacia the Psamminae (Henry, 1997). Later we will (Leguminosae),whichareP.linnavouriSˇtysin discuss the evidence for family-level relation- Africa, and Mcateella in Australia. The hosts ships of the Piesmatidae, in light of the of Miespa are unknown. primitive new fossil we describe here. Major Until now only two fossil species have been works on the family are the following: Drake known. Heissiana serafini Popov in Eocene and Davis (1958) on the morphology, an Balticamberisconsideredtobecloselyrelated overview of genera, and treatment of the tothetwosmallaustralgenera(Popov,2001). American species; Heiss and Pe´ricart (1983), Eopiesma trimerus Nel, Waller and De Ploe¨g, also on morphology, but also with detailed in lowermost Eocene (Sparnacian-aged) am- information on life histories, development, berfromtheParisbasinisconsideredtobethe andthePalaearcticspecies;Narisu(2000)ona sister group to all other piesmatids including review of their biology; and two papers by Heissiana(Neletal.,2004).Thus,thefossilwe Schaefer (1972, 1981) on relationships. report here is only the third one documented TheRecentgenera arePiesmaLepeletierde for this interesting family of true bugs, and it Saint Fargeau and Audinet-Serville, Miespa extendstheknowngeologicalageofthefamily Drake, and Mcateella Drake. The rare Asian to approximately twice what was known. genus Thaicoris Kormilev was originally (Kormilev, 1969) and later (e.g., Schaefer, MATERIALSAND METHODS 1972, 1981) placed in the Piesmatidae, but it has recently been shown to belong to the Burmese amber derives from the northern Thaumastocoridae (Heiss and Popov, 2002). province of Kachin, near Myitkyina. The Piesmaisthelargestgenuswithapproximately specimen reported here was specifically de- 31 species, and is largely Holarctic but with rivedwiththousandsofotherpiecesfromnear some African species. One common Western the villages of Huangpa and Tanai, collected Hemisphere species, Piesma cinereum (Say), by R. Cruickshank of Leeward Capital Corp. extends from North America into tropical (reviewedinGrimaldi etal.,2002).Age ofthe regions of Central and South America. amber is estimated to be Cenomanian to Late Pe´ricart (1974) classified the genus into three Albian. The Cenomanian age (ca. 98 mya) is subgenera,butmostrecentlyHeissandPe´ricart based on the geological occurrence of 21 (1997) elevated two of these (Afropiesma Mesozoic insect taxa that occur as inclusions Pe´ricart and Parapiesma Pe´ricart) to generic inBurmeseamber(Grimaldietal.,2002).The rank.Miespaisamonotypicgenusknownonly Albian age (ca. 105–100 mya) is based on one from Chile; Mcateella contains four described ammonite specimen and a modest sample of species from Australia, although numerous spores from one site (Cruickshank and Ko, undescribed species exist (G. Cassis, personal 2003). Thus, a reasonable estimate of the age commun.,2006).Thus,thefamilyisessentially of Burmese amber is approximately 100 myo. bipolar, occupying mostly the temperate re- Thepieceofamberwaspreparedaccordingto gions of the northern and southern hemi- the protocols described in Nascimbene and spheres. Silverstein (2000). Critical observation of the Host plants of the few piesmatid species minute specimen (body length 1.45 mm) re- where feeding habits are known have been quired high resolution and magnification to reviewed by Schaefer (1981). The Chenopo- view features such as scent glands, tricho- diaceae is the family that is most commonly bothria,etc. Reflected fiber optic illumination exploited as hosts, species of which are wasusedtostudythespecimenat1443witha common in salt marshes (the family also Leitz Wetzlar stereoscope and also with a includes beets and spinach). Some species in Zeisscompoundscopeatmagnificationsfrom the family Caryophyllaceae (‘‘pinks,’’ includ- 100 to 4003. We examined two specimens of ing carnations) are also common hosts. The Heissiana serafini Popov (nos. GPIH 4490, widespread species Piesma cinereum is known andparatypeGPIH2208),loanedtousbyDr. 2008 GRIMALDI ANDENGEL: CRETACEOUS PIESMATIDAE 3 Wolfgang Weitschat of the Geologisch- arisingfromunguitractorplate,nottheclaws). Pala¨ontologisches Institut und Museum at Abdomen of nymphs and adults with dorsal the University of Hamburg. This allowed us abdominal glands on terga 3–4 or 4–5 (glands to score several characters not mentioned in remain functional in adults); spiracles 2–6 in the original description of that species. dorsal position (pair 6 sometimes in submar- ginalposition);sternumVandVIwithtricho- SYSTEMATICS bothria anterior to spiracle, except absent or veryhighlyreducedinMiespa,Mcateella,and Family PIESMATIDAE Amyot and Cretopiesma (and perhaps also Heissiana and Audinet-Serville, 1843 Eopiesma); female sternum VII completely divided into hemisternites; ovipositor lanceo- Piesmides Amyot and Audinet-Serville, 1843: 300. Type late; second gonocoxopodites in inverted U genus: Piesma Lepeletier de Saint-Fargeau and position;spermathecamedian,unpaired;male Audinet-Serville,1825. genitalia symmetrical. Zosmenidae Dorhn, 1859: 41. Type genus: Zosmenus Laporte,1833. Cretopiesma, new genus DIAGNOSIS: Small (2–4 mm in length) pen- tatomomorphan bugs, some without tricho- morphan synapomorphies. Integument and DIAGNOSIS: Distinguished from all other genera of piesmatids, Recent and extinct, by corium densely areolate-punctate. Head the following features: clypeus long, protrud- roughlytransverse;compoundeyespositioned ing, with a prominent median carina that posteriorly, roughly contiguous with prono- extends to middle of frons; lack of ‘‘jugal’’ tum; ocelli present in macropterous forms, appendices/lobes; rostrum about as long as absentinbrachypterousandsubmacropterous head, inserted far from clypeal apex, enclosed forms; ‘‘jugal’’ appendices/lobes present and by bucculae at base; pronotum with pair of elongate (primitively absent in Cretopiesma); four antennomeres; mandibular plates strong- paramedian carinae, posterior margin slightly ly produced, reaching apex of clypeus in concave; mesoscutellum very large (length moderngenera(unknownforTertiarygenera, 0.213 the body length); coxae of each pair not produced in Cretopiesma); labium four- widely separated; corium venation distinctive, segmented; bucculae present at base of ros- whereveinsSc,R+M,andCuarenotfusedin trum. Pronotum subquadrate and explanate, a vein that runs parallel and proximal to the with distinct longitudinal carinae (absent in margin of the membrane and corium, instead the Eocene genus Eopiesma), without collar, with two transverse veins; membrane without calli distinct; propleura with distinct cavities ‘‘sutural area’’. beneath paranota; prosternum with depres- TYPE SPECIES: Cretopiesma suukyiae, new sion for reception of rostrum. Mesoscutellum species. greatly exposed and generally small except ETYMOLOGY: FromPiesma,thetypegenus primitively greatly enlarged in Cretopiesma; of the family; and from the Latin creta, mesosternum with depression for reception of meaning ‘‘white earth’’ or ‘‘chalk’’, which rostrum except in Miespa and Cretopiesma. refers to deep, chalky deposits in England Metapleuralscentglandostiolepresent(prim- that originally defined the Cretaceous Period itivelysoinCretopiesma)orvestigial(allother (145–65 mya). genera). Hemelytral corium areolate; mem- brane reduced, nearly absent, or present with Cretopiesma suukyiae, new species three or four nebulous veins and no cells; venation of corium (when present or discern- Figures 1–3 able) variable. Hing wing (when present) with Sc absent; R and M separated distally. Legs Piesmatidaesp.:Grimaldietal.,2002:41,fig.25e. unarmed; coxae close together, except widely separated in Cretopiesma; coxal cavities open; DIAGNOSIS: As for the genus (see above). tarsi dimerous (trimerous in Eopiesma); pre- DESCRIPTION: Based on unique female tarsuswithpaired,leaflikepseudopulvilli(i.e., specimen; small, body flattened, length 4 AMERICAN MUSEUMNOVITATES NO. 3611 Fig.1. Photomicrographsofholotype(AMNHBu958)ofCretopiesmasuukyiae,newgenusandspecies, with dorsal habitus in center. A. Head, dorsal view. B. Detail of corium. C. Detail of wing membrane. D. Protarsus.E.Tipof scutellum. F.Terminalia, ventral view.A, B, C,E, Fto same scale. 1.45 mm.Head:Wide,insertedintoprothorax face of head areolate. Bucculae short, extend- uptoventralmarginofeyes;dorsallyareolate; ed from approximately middle of clypeus to prognathous. Eyes extremely convex, bare of anteriormarginofpreoculartubercles.Pairof setulae; width across eyes 0.36 mm. Ocelli large, conical preocular tubercles present, tips absent, typical of submacropterous forms. extend nearly to distal end of first antenno- Clypeuslong,protrudent,tipextendedtolevel mere. Antenna with four antennomeres; two of middle of 3rd antennomere. Clypeus with basal antennomeres short and wide, relative mediancarina,extendingfromtiptomiddleof lengths: (1) 1.0: (2) 1.1: (3) 2.9: (4) 1.5. frons. Jugal appendices absent. Ventral sur- Antennomere 3 long and thin, antennomere 2008 GRIMALDI ANDENGEL: CRETACEOUS PIESMATIDAE 5 Fig. 2. Dorsal habitusof holotypeof Cretopiesma suukyiae,new genusand species. 6 AMERICAN MUSEUMNOVITATES NO. 3611 Fig.3. DetailsofholotypeofCretopiesmasuukyiae,newgenusandspecies.A.Ventralviewofheadand thorax. B. Apexof abdomen(ventralview). C. Mesothoracic tarsus. 2008 GRIMALDI ANDENGEL: CRETACEOUS PIESMATIDAE 7 4 fusiform, with dense, long setulae at apex. brane areolate; distinct commissure between Antennalinsertionbetweenpreoculartubercle clavus and rest of corium. Membrane of andclypeus.Rostrumextendedtoleveloffore hemelytra with fine reticulations, four faint coxae (segmentation obscure). longitudinal veins with apices evanescent and Thorax: Pronotum broad (length at middle notmeeting distalmarginofwing.Membrane 0.28 mm, greatest width 0.52 mm), explanate; veins interpreted here as R, M, Cu, and PCu; trapezoidal in shape, with lateral margins latter two veins convergent but not actually diverging caudad, posterior margin slightly intersecting. Hindwingunapparentorabsent. concave(vs.slightlyconvexorflat).Pronotum Abdomen: Flat, broad; length 0.85 mm, areolate over entire dorsal surface, with two width 0.55 mm. Ventral trichobothria not large paramedial carinae extended full length apparent, or absent. Spiracles situated dorsal- ofpronotum.Carinaetaperedinthicknessand ly on paratergites II–V. Tergite VII with slightly divergent caudad; anteriorly fused numerous small spicules. Pair of spiracles on with thick transverse carina on anterior segment VII situated on small tubercles. margin of pronotum. Pronotum with pair of ParatergitesVIIIapairofsmalllobesflanking callosities lateral to carinae and in slightly paratergitesIX,whichareapicalmostappend- recessed areas. Mesoscutellum very large, ages. Paratergites IX apparently flat, with 0.31 mm in length, 0.37 mm width; dorsal outer margins finely dentate. Sternite VII surface completely areolate, with apical mar- divided, pair of gonocoxopodite 2 visible gin broadly rounded. Posterior half of scutel- beneath sternite VII, >-shaped. lum with paramedial pair of rounded depres- MATERIAL EXAMINED: Holotype (unique sions. All sternites smooth, not areolate or specimen), female, AMNH Bu958, from punctate. Prosternum with very broad rostral Kachin Province, northern Myanmar, near groove; no mesosternal groove. Propleural the town of Tanai in the Hukwang Valley. In cavities present, just anterior to fore coxae. the amber fossil collection, Division of Metasternum very broad; no scent gland Invertebrate Zoology, American Museum of channel present, but apparently with small Natural History. ostiole (scent gland opening?) anterolateral to ETYMOLOGY: MatronyminhonorofAung metacoxa. All coxae widely separated in each SanSuuKyifromBurma,the1991laureateof pair. Legs short, femur thickest podite; all the Nobel PeacePrize. Ms. Suu Kyi has spent podites devoid of spines, but femur and tibia 18 years isolated in house confinement (from covered with numerous, fine tubercles. Tarsi 1989–95,2000–02,and2003topresent)forher with two short tarsomeres, apical tarsomere promotion of democracy in Myanmar. It is slightly longer; pretarsal claws apparently fitting that a Burmese species, seemingly simple,ratherlong;pulvillilarge,slender,flat, delicate but which has beautifully endured slightly shorter than claws. for so long, be named in her honor. Wings: Hemelytra short (submacropterous form?), apices extend to apex of abdomen but DISCUSSION not beyond; length 0.76 mm, greatest width 0.28 mm. Apex of hemelytron broadly round- On the surface, the many unique or highly ed, not narrowed. Corium occupies approxi- unusual features of Cretopiesma listed in the mately half the hemelytral surface; entire genericdiagnosismightsuggestitsplacementin coriumareolate,exceptveins.Veinsthickened, a family other than Piesmatidae. However, at heavily sclerotized. Vein C short, occupies least some of these features are plesiomorphic 2/3 basal half of hemelytron. Sc very short, forthefamilyandothersautapomorphic.More branches off main stem of Cu, meets C (not importantly, features of Cretopiesma that are R+M), length ca. 0.253 wing length. Two diagnostic for Piesmatidae are the following: thick transverse veins present, one connecting head, thorax, and corium with the same, apex of Sc and Cu (near apex of clavus); distinctive form of areolation (e.g., fig. 4A); a another a slightly V-shaped crossvein near short, stout second antennomere (cf. figs. 2, middle of wing connecting C and Cu. Clavus 4C); pronotum explanate and with dorsal narrow, apex very slender and acute, mem- carinae;presenceofpropleuralcavities(figs. 3, 8 AMERICAN MUSEUMNOVITATES NO. 3611 Fig.4. ScanningelectronmicrographsofPiesmaspp.(A,C:Arizona;B,D:SouthAfrica).A.Habitus, dorsalview.B.Habitus,ventralview.C.Headandanterior pronotum,dorsalview.D.Headandanterior thorax, ventral view. 2008 GRIMALDI ANDENGEL: CRETACEOUS PIESMATIDAE 9 Fig.5. ScanningelectronmicrographsofPiesmasp.(SouthAfrica).A.Leftanteriorportionofthorax (ventral view), showing propleural cavity. B. Trichobothrial pad. C. Pretarsus, showing well-developed pulvilli. D.mesopleural fold nearcoxa. 5A);andthestructureofthefemaleterminalia, small, flattened body; proportions of the four where sternum VII is entirely divided into antennomeres; preocular tubercles large and hemisternites, the ovipositor lanceolate, and protuberant; hemelytron with basal half cori- the second pair of gonocoxopodites are an in- aceous,apicalhalfmembranouswithfourlight verted U (fig. 3). Further features of Creto- veins (fig. 2); two tarsomeres present, with piesma that are consistent with Piesmatidae pretarsushavingapairoflarge,leaflikepulvilli (though not exclusive to this family) are the (fig. 1D). 10 AMERICAN MUSEUMNOVITATES NO. 3611 RELATIONSHIPSWITHIN PIESMATIDAE TABLE1 DataMatrix for PhylogeneticAnalysis of An attempt was made to investigate rela- Piesmatidae tionships among living and fossil genera by (see textfor descriptionof characters) expanding upon and revising those characters employed by Schaefer (1972, 1981). In addi- taxa characters tion, several new characters were included to 11111111112222 accommodate the features found in the one 12345678901234567890123 Cretaceous (herein) and two Eocene (Nel et Piesma al., 2004; Popov, 2001) fossils. Twenty-three (Piesma) 10111110$11111111011111 characters were identified and coded for (Parapiesma) 11111110211111111011111 cladistic analysis. In the following list apo- (Afropiesma) 10111110011111111011111 morphiesaredescribedfirst (codedas1inthe Miespa 10110000201101?11011011 matrix: table 1), succeeded by brief notes on Mcateella 10110000201111011211011 Heissiana 10010000101111?1111?011 the distribution of the trait and its plesio- Eopiesma 10010001?01???0011?0111 morphic condition. Outgroups included the Cretopiesma 00100110010000010000011 basal pentatomomorphan family Aradidae. Outgroup* 00000000000000000000000 *Theoutgroupwasgeneratedfromplesiomorphicstates HEAD: inferredbycomparisonacrossbasalpentatomorphs. 1. Clypeus reduced, not projecting. This $subsetpolymorphism(50/1) feature is found in all Recent piesmatid species and in the Tertiary fossils. 6. Third antennomere very slender and Cretopiesma plesiomorphically has a significantly longer than second antenno- stronglyprojectingclypeussimilartothat mere, which is a feature found in Piesma of many Aradidae (cf. figs. 2, 6A). and Cretopiesma (figs. 2, 4B). In the 2. Preocular tubercles bifid, with small plesiomorphic condition the third anten- secondary pair lateral to the large pair nomere is barely longer or even shorter found in Recent and extinct species. This than antennomere 2, which is found in feature is autapomorphically present in the austral and Tertiary fossil genera. Piesma (Parapiesma); all other species 7. Position of head porrect (apomorphic) have the single large pair. versus declivant, the apomorphic state 3. Rostrumshort,apexextendingnofarther occurring in Piesma and Cretopiesma. than the level of procoxae. Plesiomor- THORAX: phically,therostrumextendswellbeyond this level, a condition found in the fossil 8. Absence of pronotal callosities (or calli): generaHeissianaandEopiesma,andinP. this state is hypothesized to be apo- (Parapiesma) kolenatii (Fieber), P. pupu- morphic (i.e., a loss), since the presence la Puton, and P. tenellum Horvath. of callosities is widespread in Heterop- 4. ‘‘Jugal’’ lobes3 absent, which is a feature tera. This presumably occurs just in the found in Cretopiesma. All other piesma- fossil Eopiesma, but the structure can be tids have well-developed jugal lobes difficult to discern even in amber fossils (figs. 4C, D). (and the bubble above the pronotum in 5. ‘‘Jugal’’ lobes long, projecting well be- the unique holotype [Nel et al., 2004: 46, yondtheclypeusinadults,whichisfound fig.1]mightobscurethisfeature).Likeall in Piesma s.l. Plesiomorphically, the other features of Eopiesma that we apices of the jugal lobes are at the same scored, we relied on the observations by level as the apex of the clypeus. Nel et al. (2004). 9. Pronotumwithshort,mediancarina(e.g., 3This is an adjectival form of the ‘‘juga’’ (extensions fig. 4A): Plesiomorphically this structure lateraltotheclypeus)andshouldnotbeconfusedwiththe is absent (0); apomorphically with small more widespread application of this term for the membranous lobe formed by the jugum in the posterior or faint carina (1), or with a well- baseoftheinsectwing. developed, longer carina (2). This feature