The Auk 117(4):964-970, 2000

TINY -LIKE FROM THE MIDDLE OF MESSEL (GERMANY)

GERALD MAYR • ForschungsinstitutSenckenberg, Sektion fiir Ornithologie,Senckenberganlage 25, D-60325 Frankfurta.M., Germany

ABSTRACT.--Tinyhoopoe-like birds of the extinctfamily Messelirrisoridaeare amongthe predominantsmall perching birds in the Middle Eocene(ca. 49 million yearsago) avifauna of Messel(Hessen, Germany). Members of the Messelirrisoridaeare the earliest-knownrep- resentativesof the hoopoe/wood-hoopoelineage and are sistertaxa of recentUpupidae ()and Phoeniculidae(wood-hoopoes). Outgroup comparison with the Messelirri- soridaefacilitates character-state analysis within the Phoeniculidaeand Upupidae.In this study,I describea new ,Messelirrisor grandis, which is the largestspecies of the Mes- selirrisoridaeknown so far. Received31 August1999, accepted 28 April 2000.

THE FORMER OPENCAST oil-shale mine "Gru- daepredominate. So far, two speciesin a single be Messel" is located a few kilometers north- genushave beendescribed, Messelirrisor halcy- eastof Darmstadt in Hessen,Germany. Accord- rostrisand M. parvus(Mayr 1998). Both are ing to the currentlyfavored hypothesis, the de- known from severalcomplete articulated skel- positsof Messeloriginated in a deepcrater lake etons preserved on slabs, and both are of tectonicorigin about49 million yearsago in small,more diminutiveeven than many recent the LowerMiddle Eocene.The sitehas yielded hummingbirds(Fig. 1). Here,I describea third a large number of vertebratefossils in an ex- speciesfrom the Messelirrisoridae,the largest ceptionalstate of preservation;in many cases, known so far. the remains of former soft tissues and stomach The specimensare depositedin the contentshave been preserved (see Franzen Geiseltalmuseum,Halle, Germany(GMH), the 1985,Schaal and Ziegler 1988).In 1995,Messel ForschungsinstitutSenckenberg, Frankfurt was declareda world heritagesite by UNESCO. a.M., Germany (SMF), and in the Staatliches In terms of the number of individual skele- Museum fiir Naturkunde,Karlsruhe, Germany tons and the number of species,birds are (SMNK). Measurementsreported below rep- among the most abundant land vertebrates resentthe overalllength along the longitudinal found in Messel. In recent decades, several axis. Anatomical terminology follows Baumel hundredbird skeletonswere discovered,many and Witruer (1993)unless indicated otherwise. of themcomplete and articulated.The avifauna is very diverse,and thusfar about50 avianspe- SYSTEMATICS cieshave been identified. Among these are ibis- es (Peters1983), swifts (Peters1985, Mayr and Hoopoe-likebirds comprisetwo recentfam- Peters1999), parrots (Mayr and Daniels 1998), ilies, the PalearcticUpupidae (hoopoes)and and frogmouths(Mayr 1999).Contrary to near- the African Phoeniculidae(wood-hoopoes), ly all other sitesthat haveyielded fossilbirds, and generallyare classifiedtogether with roll- even extremely small skeletonsare pre- ers, ,bee-eaters, todies, and mot- servedin Messelin greatnumbers. motsin the orderCoraciiformes (see Sibley and Passeriformsare completelyabsent in theEo- Ahlquist1990:336-348). Yet, because the mono- ceneavifauna of the NorthernHemisphere, at phyly of thisorder has never been convincingly which time the ecologicalniches for small established with derived characters, I use the perchingbirds were occupiedby representa- term Upupiformes(sensu Feduccia 1977, Sibley tives of other avian taxa (Harrison 1979, Olson and Ahlquist 1990)for hoopoe-likebirds. 1989, Feduccia1996). In Messel,tiny hoopoe- Monophylyof the Upupiformesis supported like birds of the extinct family Messelirrisori- by the following charactersthat are unique among.neognathous birds: shaft of ulna with E-mail: [email protected] projection distal to cotyla dorsalis (Fig. 2, no.

964 October2000] Hoopoe-likeBirds from Messel 965

1

Moraotus momotus Upupa epops

FIG. 2. Proximal ulna of Momotusmomotus (Mom- otidae,left) and Upupaepops (right). (1) Projectionbe- low theprocessus cotylaris dorsalis that is synapo- rnorphic for the Messelirrisoridae,Upupidae, and Phoeniculidae. Scale bar = 5 mm.

irregularlyshaped (unique among neognath- ous birds); (3) spina externa and spina interna of sternum fused to form a spina communis (onlyin very few otherneognathous birds, e.g. Meropidaeand someBucerotidae); (4) sternum with onlyone pair of incisions(the two pairsof the Messelirrisoridaegenerally are considered to be plesiomorphicwithin neognathousbirds; e.g. Olson 1987);and (5) phalanxproximalis FIG. 1. Messelirrisorparvus (SMNK PAL 3802), digiti majoris hooked (among other recent slightlydisarticulated with detachedskull and cer- neognathousbirds only in Galbulidaeand Buc- vical vertebrae.Specimen is coatedwith ammonium conidae; Fig. 3, no. 3). Recent upupids and chloride to enhance contrast. Scale bar = 10 mm. phoeniculidsalso share a derived stapedial morphology(Feduccia 1975). 1); carpometacarpuswith osseousridge from The new speciesdescribed below exhibits all ventral margin of os metacarpaleminus to pro- of the above-mentioned derived characters of cessuspisiformis (Fig. 3, no. 1); and caudal the Upupiformesand lacksthose of the Upu- margin of os metacarpaleminus (carpometa- pidae and Phoeniculidae.Especially the hu- carpus)undulated (only slightlyin Messelirri- merusand the carpometacarpusof the Messe- soridae;Fig. 3, no. 2). Apart from their much lirrisoridaeare highly characteristicand can smaller size, messelirrisoridsclosely resemble hardlybe mistakenwith thoseof anyother avi- Upupidaeand Phoeniculidaein manyother os- an taxon(see below). Apart from its largersize, teologicalfeatures: (1) long,pointed, and at the the new speciesvery closelyresembles the oth- basedorsoventrally high beak;(2) presenceof er speciesof the genusMesselirrisor in its os- largeprocessus retroarticulares on the mandi- teology. ble; (3) shapeof the extremitasomalis of the furcula;(4) absenceof an apophysisfurculae; Messelirrisorgrandis sp. nov. (5) stouthumerus; (6) proportionsof limb ele- ments;and (7) longhallux. Holotype.--SMNK PAL 3803 (sternum, pec- The upupidsand phoeniculidsare united to toral girdle and both wingson a slab;Fig. 5). the exclusion of the Messelirrisoridae because Diagnøsis'--Messelirrisørgrandis is thelargest the formertwo familiesshare the following de- speciesof the Messelirrisoridaeknown so far rived characters:(1) margo medialisof cora- (Table1). It is further distinguishedfrom M. coid with distinctmedially projectingprocess parvusand M. halcyrostrisin the slightlymore (Figs.4A-C, no. 1; uniqueamong neognathous cranially situatedprocessus pisiformis of ); (2) processuslateralis of coracoidvery carpometacarpus. 966 GERALDMAYR [Auk, Vol. 117

Messelirrisorhalcyrostris

Upupa epops

FIC.3. Left manusof Messelirrisorhalcyrostris (after Mayr 1998)and Upupaepops. (1) Ridgefrom the ven- tral side of the os metacarpaleminus to the processuspisiformis; (2) undulatedcaudal margin of the os metacarpaleminus; (3) hookeddistal end of phalanxproximalis digiti majoris.Scale bar = 5 mm.

Typelocality.--Messel near Darmstadt (Hes- dorsoventrally,and the culmen is slightly sen, Germany). curved.The narial opening is longand slit-like, Typehorizon.--Lower Middle Eocene(Legen- and the rami mandibulae are wide dorsoven- dre and L•v•que 1997). trally. Measurementsofholotype.--Coracoid, about 12 Like in other messelirrisorids,the extremitas mm; left humerus,19.3 mm, right humerus, omalisof the furculais rhombicin shape(more 20.1 mm; ulna, about24 mm; carpometacarpus, round in recentUpupiformes), and the scapus 10.7 mm (Table 1). claviculaeis slender.The scapulais shortand Referredspecimen.--SMF-ME 600, a largely straight.The acromionis alsoshort and bears completebut poorlypreserved skeleton on two a small projectionon its ventral side. The ex- slabs,from the type localityand horizon(Fig. tremitasomalis of the coracoidis hidden by 6). overlyingbones in the type specimen.The pro- Measurementsof referred specimen.--Skull, cessus lateralis of the extremitas sternalis is about 41.5 mm; coracoid, about 12 mm; hu- narrow but long. A small notchoccurs on the merus, about 20 mm; ulna, about 23 mm; car- medial side of the extremitas sternalis. pometacarpus,about 10 mm; tibiotarsus,about The sternumis slightlylonger than wide and 19 mm; tarsometatarsus, about 10.4 mm. bearsshort processus craniolaterales. Its lateral Etymology.--Thespecific name has been de- marginsare somewhatcurved, and the margo rived from Latin grandis,large, and refersto costalis is short. Like in other messelirrisorids, thelarge size of thenew species compared with the othertwo speciesof messelirrisorids. the margocaudalis bears two pairsof incisions, whereasrecent Upupiformes have only one pair The incisionson the right sideof the ster- REMARKS num are nearlyequal in depth(about one-third The skull is preservedin the referredspeci- the lengthof the sternum),and on the left side men SMF-ME600, but owing to the flattening the incisuramedialis is slightlydeeper. The in- of the bones,details of its morphologycan cisurae laterales are narrower than the incisu- hardly be discerned.In its shape,however, it rae mediales. The trabeculae laterales are wide, matches well with the skull of other messelir- and the trabecula mediana is triangular in risorids.This is especiallytrue for the longand shape. pointedbeak, which is about1.5 timeslonger The humerusis shortand stoutwith a large than the cranium.The beakis high at its base proximal end and a slightly curved, robust October2000] Hoopoe-likeBirds from Messel 967

Messelirrisor Upupa Messelirrisor FIG.4. Right coracoidof (A) Messelirrisorparvus (after Mayr 1998),(B) Upupaepops, and (C) Phoeniculus sp. Distal end of the right humerusof (D) Messelirrisorsp. (GMH L-9-1969).(1) Processon the medial side of the extremitassternalis; (2) processussupracondylaris dorsalis; (3) epicondylusdorsalis; and (4) osseous bridge connectingthe processusprocoracoideus with the faciesarticularis clavicularis. Scale bar = 5 mm. shaft. The tuberculum dorsale bears a shallow and bears a pit-like depressionon its medial depression.The distal humerus of messelirri- surface. soridsis very characteristicin that the epicon- The ulna exceedsthe humerusin length.On dylus dorsalisprotrudes unusually far laterally the left ulna of the type specimen,a projection to form a small tuberclenext to the condylus below the processuscotylaris dorsalisis visi- dorsalis(Fig. 4D, no. 3). This protrudingepi- ble, whichis synapomorphicfor the Upupifor- condylusdorsalis also is clearly visible in the mes (Fig. 2, no. 1). The tuberculumcarpale is type specimenof M. grandis.Like in othermes- pointed and bears a depressionon its distal selirrisorids, the processussupracondylaris surface.Like in recent Upupiformes,low pa- dorsalisis a small tubercleabove the epicon- pillae remigalesare present.Other details of dylus dorsalis.The sulcusscapulotricipitalis is the ends of the ulna are not visible. The distal distinct.The processus flexorius reaches slight- end of the radius bears a single,wide sulcus ly farther distally than the condylusventralis tendinosus. The carpometacarpusis well preservedin the typespecimen and closely resembles that of other messelirrisorids,although the processus

ß pisiformisis shifted slightly farther cranially than in the other speciesof Messelirrisor.The processusextensorius of the os metacarpaleal-

TABLE1. Length (mm) of some wing elementsin the threeknown species of messelirrisorids(SD in parenthesesfor M. parvus).

Carpo- Coracoid Humerus Ulna metacarpus Messelirrisorgrandis (holotype) ca. 12 19.3/20.1 ca. 24 10.7 Messelirrisorhalcyrostris (n = 1) 9.3 14.6 17.2 8.0 FIG. 5. Messelirrisorgrandis, holotype (SMNK Messelirrisor parvus (n = 7) PAL 3803).Specimen is coatedwith ammoniumchlo- ride to enhance contrast. Scale bar = 8 mm. 8.8 (0.3) 12.9 (0.6) 16.3 (0.7) 7.0 (0.4) 968 GERALDMAYR [Auk, Vol. 117

the Lower Eoceneof England,in Middle Eo- cenedeposits of the GeiselValley of Germany, and in theUpper Eoceneof France(Mayr 1998). In contrast, the fossil record of the two recent families,Upupidae and Phoeniculidae,is more scantyand comes from much younger deposits. Ballmann (1969) described remains of the Phoeniculidae from the Lower of Ger- many;the earliestrecord of theUpupidae is an extinctspecies from the Quaternaryof St. He- lena Island (Olson 1975). Ballmann (1969) also assigneda smallhumerus from the earlyMio- cene of France to the Phoeniculidae. This bone (Milne-Edwards1867-71: plate 176,figures 8 to 13) is muchsmaller than the humerusof any FIG. 6. Messelirrisorgrandis, referred specimen recent wood-hoopoe(according to Ballmann (SMF-ME600). Specimenis coatedwith ammonium [1969]it measuresonly 19.5mm). Its distalend chlorideto enhancecontrast. Scale bar equals10 mm. resembles the distal humerus of the Messelir- risoridaein the dorsallyprotruding epicondy- lus dorsalis, and without additional skeletal el- ulare is fairly straightand protrudes cranially. ementsits assignmentto the Phoeniculidaere- The fossainfratrochlearis and the faciesliga- mains uncertain. mentalis interna (terminologyafter Ballmann Becauseof the concordancein the shapeof 1969)are markeddepressions. The osmetacar- pale minus is stronglybowed; thus, the spa- theirlong, robust and pointed beaks, members of the Messelirrisoridaeprobably had a diet tium intermetacarpaleis very wide, like in re- cent hoopoesand wood-hoopoes.A distinct similarto that of extantupupiforms, consisting ridge runs from the caudalend of the os me- mainly of insectsand othersmall invertebrates. tacarpaleminus to the processuspisiformis, The presenceof large processusretroarticula- which is synapomorphicfor the Upupiformes, reson the caudal end of themandible (see Mayr and the ventralmargin of the os metacarpale 1998)suggests that messelirrisoridsalso were minus is slightly undulated.The symphysis adaptedto gaping,i.e. to openingtheir beak in the substrate in a similar manner to that of their metacarpalisdistalis is very narrow. The phalanxproximalis digiti majorisbears recentrelatives (see 1984).The speci- a marked fossa ventralis, and its distal end is mens of Messelirrisorparvus differ distinctlyin not hooked like in recentUpupiformes. The the relativelengths of theirbeaks, and thebird phalanxdigiti minorisis not aselongated as in in Figure 1 is one of the rather short-beaked the recentUpupiformes. The pelvis and hind specimens.This differencemight result from limbs are preservedonly in the referredspec- agedifferences or from sexualdimorphism, as imenbut are too crushedfor detailedanalysis. in some recent Phoeniculidae in which the The proportionsof the legs correspondwith beaksof malescan be 20%longer than those of those of other messelirrisorids. The tarsometa- females (Ligon and Davidson 1988). Too few tarsusis short,and as in otherupupiforms the specimenswith completebeaks are known 'halluxis fairly long. from M. halcyrostrisand M. grandisto draw Remainsof the remigesare preservedin the meaningfulcomparisons. type specimenand the referredspecimen, but Because the Messelirrisoridae is a sister tax- they do not allow for meaningfulmeasure- on of the recentUpupiformes, outgroup com- ments. parisons with the Eocenefamily facilitates character-stateanalysis within the Phoeniculi- DISCUSSION dae and Upupidae.The frontalsof the Upupi- dae, for example,are unusually wide between The Messelirrisoridaeare by far the earliest- the orbitae,and an osseousbridge connects the known representativesof the Upupiformes. processusprocoracoideus of the coracoidwith Isolated bones of this taxon were also found in thefacies articularis clavicularis (Fig. 4B, no. 4). October2000] Hoopoe-likeBirds from Messel 969

These characters are absent in the Messelirri- feeding apparatusin the avian ordersCoraci- soridae and therefore are probably autapo- iformes and Piciformes. Bulletin of the British morphicfor hoopoes.For the samereason, the Museum (Natural History) ZoologicalSeries 47: 331-443. very slenderextremitas sternalis of the furcula FEDUCCIA,g. 1975.The bony stapes in the Upupidae and the low crista deltopectoralisof the hu- and Phoeniculidae: New evidence for common merus seem to be derived characters of the ancestry.Wilson Bulletin 87:416-417. Phoeniculidae. FEDUCCIA,A. 1977. A model for the evolution of Recenthoopoes and wood-hoopoesare es- perchingbirds. Systematic Zoology 26:19-31. peciallydistinguished in their meansof loco- FEDUCCIA,g. 1996.The originand evolution of birds. motion.Whereas upupids perch and roost in Yale University Press,New Haven, Connecticut. treesbut mainly forageon the ground,phoen- FRANZEN,J. L. 1985. Exceptionalpreservation of Eo- iculids are specializedfor climbingtree trunks. cene vertebratesin the lake deposit of Grube As in other scansorialbirds (e.g.woodpeckers Messel.Philosophical Transactions of the Royal and woodcreepers),the trochleametatarsi II! of Societyof London SeriesB 311:181-186. the tarsometatarsusof phoeniculidsbears a HARRISON,C. J. O. 1979. Small non-passerinebirds deep furrow that is absentin messelirrisorids of the Lower Tertiary as exploitersof ecological nichesnow occupiedby passerines.Nature 281: and upupids(Mayr 1998).The fairly shorttar- 562-563. sometatarsusand the long and curvedclaw on LEGENDRE,S., AND E LI2V•QUE.1997. Etalonnagede the hallux of messelirrisorids indicate that the l'•chellebiochronologique mammalienne du Pa- latterdid not forageregularly on the groundas l•oggne d'Europe occidentale:Vers une int6gra- do recentupupids. tion a l'6chelleglobale. Pages 461-473 in Actes Exceptfor Maurer and Raikow (1981), most du CongrgsBiochroM'97 (J.-P. Aguilar, S. Le- recent authorshave consideredhornbills (Buc- gendre,and J. Michaux,Eds.). M6moires et Tra- erotidae)to be the closestliving relativesof the vaux de l'Ecole Pratiquedes Hautes Etudes,In- Upupiformes (e.g. Burton 1984, Sibley and stitut de Montpellier 21. Ahlquist 1990). The earliest certain record of LIGON, D., AND N. C. DAVIDSON.1988. Phoeniculi- the Bucerotidae is from the Middle Miocene of dae,wood-hoopoes. Pages 356-370 in The birds Morocco (Brunet 1971), but the Messelirrisori- of , vol. 3 (C. H. Fry, S. Keith, and E. K. Urban, Eds.). Academic Press,London. dae provides a minimum age of 49 million MAURER,D., AND g. J. RAIKOW.1981. Appendicular years for the branchingof the Upupiformes from their sister taxon. nayology,phylogeny, and classificationof the avian order (including Trogoni- formes). Annals of the Carnegie Museum 50: ACKNOWLEDGMENTS 417-434. MAYR, G. 1998. "Coraciiforme" und "piciforme" I thankW. Munk (SMNK), E. Frey (SMNK), andS. Kleinv6gel aus dem Mittel-Eozan der Grube Schaal(SMF) for loaningspecimens and S. Trankner Messel (Hessen, Deutschland). Courier For- (SMF)for takingthe photographs. I also thank J. Cra- schungsinstitutSenckenberg 205:1-101. craft, R. Zink, and an anonymousreviewer for com- mentson the manuscript. MAYR,G. 1999.Caprimulgiform birds from the Mid- dle Eoceneof Messel (Hessen,Germany). Jour- nal of VertebratePaleontology 19:521-532. LITERATURE CITED MAYR, G., AND M. DANIELS.1998. Eocene parrots BALLMANN,P. 1969.Die V6gel ausder altburdigalen from Messel(Hessen, Germany) and the London Spaltenffillungvon Wintershof(West) bei Eich- Clay of Walton-on-the-Naze(Essex, England). statt in Bayern.Zitteliana 1:5-60. SenckenbergianaLethaea 78:157-177. BAUMEL,J. J., AND L. M. WITMER.1993. Osteologia. MAYR,G., ANDD. S. PETERS.1999. On the systematic Pages45-132 in Handbook of avian anatomy: positionof the Middle Eoceneswift Aegialornis Nomina anatomica avium (J. J. Baumel, A. S. szarskiiPETERS 1985 with descriptionof a new King, J.E. Breazile,H. E. Evans,and J. C. Vanden swift-like bird from Messel (Aves, Apodifor- Berge,Eds.). Publications of theNuttall Ornitho- mes).Neues Jahrbuch f/Jr Geologie und Palaon- logicalClub No. 23. tologie,Monatshefte 1999:312-320. BRUNET,J. 1971. Oiseaux miocgnes de Beni Mellal MILNE-EDWARDS, A. 1867-71. Recherches anato- (Maroc);un comp16menta leur 6tude.Notes M6- miques et pa16ontologiquespour servir a moireset ServiceG6ologique (Marocco) 31:109- l'histoire des oiseaux fossiles de la France. Victor 111. Masson et ills, Paris. BURTON,P. J. K. 1984.Anatomy and evolutionof the OLSON,S. L. 1975.Paleornithology of St. HelenaIs- 970 GERALDMAYR [Auk, Vol. 117

land, Atlantic Ocean. Smithsonian Con- PETERS,D. S. 1985. Ein neuer Segler aus der Grube tributions to Paleobiology23:1-49. Messelund seineBedeutung ffir den Statusder OLSON,S. L. 1987.An early Eoceneoilbird from the Aegialornithidae(Aves: Apodiformes).Senck- River Formationof Wyoming (Caprimul- enbergianaLethaea 66:143-164. giformes:Steatornithidae). Documents des La- SCHAAL,S., AND W. ZIEGLER.1988. Messel-Ein Schau- boratoiresde G6ologiede Lyon 99:57-69. fenster in die Geschichte der Erde und des Le- OLSON,S. L. 1989. Aspectsof global avifaunal dy- bens.Kramer, Frankfurt, Germany. namicsduring the Cenozoic.Pages 2023-2029 in SIBLEY,C., ANDJ. E. AHLQUIST.1990. Phylogeny and Acta XIX CongressusInternationalis Ornitholo- classificationof birds: A study in molecularevo- gici (H. Ouellet, Ed.). Ottawa, Ontario, 1986.Na- lution. Yale University Press,New Haven, Con- tional Museum of Natural Sciences, Ottawa. necticut. PETERS,D. S. 1983.Die "Schnepfenralle"Rhynchaeites messelensisWittich 1898 ist ein Ibis. Journal ffir Ornithologie124:1-27. Associate Editor: R. M. Zink