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The Scleral Ossicles of Opisthocomus and Their Phylogenetic Significance

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The Scleral Ossicles of Opisthocomus and Their Phylogenetic Significance THE SCLERAL OSSICLES OF OPISTHOCOMUS AND THEIR PHYLOGENETIC SIGNIFICANCE KEVIN DE QUEIROZ AND DAVID A. GOOD Museumof VertebrateZoology and Department of Zoology,University of California, Berkeley,California 94720 USA ABSTRACT.--Driedscleral rings of Opisthocomus,Galliformes, Cuculiformes, and other birds were examined to determine the pattern of ossicleoverlap in Opisthocomusand its bearing on the phylogeneticrelationships of this taxon. Although Opisthocomusshares a derived numberof 12scleral ossicles with cuculidCuculiformes, the patternof ossicleoverlap differs. Nevertheless,fewer modificationsare required to derive the number and pattern of ossicles in Opisthocomusfrom the conditionsin cuculidor musophagidCuculiformes than from the conditionsin any galliform.Our findingsalso indicate that the scleralrings of birds,unlike thoseof lizards, often do not conserveoverlap relationsbetween adjacentossicles during phylogeny.Received 2 March 1987,accepted 23 July1987. THE phylogenetic relationships of the Hoa- lap in the scleralrings of larger samplesof Opis- tzin (Opisthocomushoazin) have been the subject thocomus,Cuculiformes, Galliformes, and other of a long-standingcontroversy in systematicor- relevant avian taxa. Our findings have impli- nithology. An enigmatic inhabitant of the cations both for the relationships of Opis- flooded forestsof Amazonia, Opisthocomushas thocomus and for the manner in which scleral been regardedas most closelyrelated to many rings evolve. avian taxa, but most commonly to either Cu- culiformes or Galliformes (Olson 1985; re- MATERIALS AND METHODS viewed by Sibley and Ahlquist 1972,1973). One characterthat hasbeen usedto supporta close Twenty-four scleralrings from 14 Opisthocomusin- relationshipbetween the Opisthocomusand Cu- dividuals were comparedwith rings from 42 galli- form and 36 cuculiformspecies representing all of cullformesis the morphology of the sclerotic the recognizedfamilies, subfamilies,and tribes (Mo- ring, a ring of small bones that developswithin tony et al. 1975) in those groups (Table 1). To un- the sclerain the cornealhemisphere of the eye derstand variation in scleral ossicleoverlap patterns in birds and many other vertebrates(Edinger for a given number of ossicles,we also examined 1929). Lemmrich (1931) found that the scleral representativesof other avian groupswith the same ring of Opisthocomusconsists of 12 ossiclesper number of ossiclesas Opisthocomus(Spheniscidae, Su- eye, which is lower than the 13-16 ossicleshe lidae, Psittacidae,and Todidae). found in 10 speciesof cracidand phasianidGal- We examinedonly the dried, detachedscleral rings liformes (all of which showed a modal number from museumskeletal specimens; no rings were ex- of 14) but is identicalto that found in a single amined in situ.In many casesscleral ossiclepatterns couldbe distinguishedin theserings without further cuculiform, Cuculus canorus. preparation, but in others adherent connectivetissue In addition to ossiclenumber, the pattern in was removed.This was accomplishedby immersing which the scleralossicles overlap varies among the rings in water or ethanol to soften the adherent avian taxa (Lemmrich 1931, Curtis and Miller tissue,which wasthen removedwith forceps.Because 1938).Because the samenumber of ossiclesmay we used only detachedscleral rings, the side of the havebeen derived independently, simple counts headfrom which eachring camehad to be inferred. can be misleading. The pattern of ossicleover- We used the patternsin the sameor closelyrelated lap providesevidence about ossicle homologies taxaobserved by Lemmrich(1931) in conjunctionwith and hence about cases in which the same num- the fact that the widestossicles occur at the tempo- ber of ossicleshas been derived through the rodorsaledge of the ring (best seen in Fig. 1D) to loss of different individual ossicles. determinewhether a given ring was from the right or left side. Although the pattern of scleral ossicleover- We followed Lemmrich's (1931) conventions for lap is known for many birds, it has been un- numberingossicles and describingpatterns of ossicle known for Opisthocomus.We compared the overlap.Lemmrich recognized two basicpatterns of numbers of ossiclesand their patterns of over- ossicleoverlap, which he designatedTypes A and B. 29 The Auk 105:29-35. January1988 30 DEQUEIROZ AND GOOD [Auk,Vol. 105 A 7+ 9+ D E F Fig. 1. Modal patternsof scleralrings in Opisthocomus,Galliformes, and Cuculiformes.(A) Opisthocomus hoazin(Opisthocomidae), (B) Alecturalathami (Megapodiidae), (C) Aburriaaburri (Cracidae), (D) Numidameleagris (Phasianidae),(E) Crotophagaani (Cuculidae), (F) Tauracohartlaubi (Musophagidae). All ringsare from the right side, seen in corneal view. Scale equals 5 mm. In Type A two ossiclesin eachring overlap, and two mined by outgroupcomparison (e.g. Maddisonet al. others are overlapped by, the immediately adjacent 1984). ossicles;all othershave one edge aboveand one be- neath the adjacentossicles (Fig. 1A, C-F). Lemmrich RESULTS pointed out that the most dorsal ossiclein Type A rings alwaysoverlaps both its neighbors,and he re- The distribution of scleral ossicle number and ferred to suchoverlapping ossicles as "+" elements. patternin Galliformes,Cuculiformes, and Opis- Approximatelyopposite this dorsal "+" element is thocomusis listed in Table 1. Opisthocomus(Fig. another "+" element that he designatedossicle num- 1A) showed a modal number of 12, with a range ber 1. He counted ossiclesaround the ring postero- from 11 to 13. Galliformes(Fig. 1B-D) showed dorsallyfrom this ventral "+" element, clockwiseon a modal number of 14, with only about 15% of the right ring and counter-clockwiseon the left. He then recordedthe positionsof the "+" elementsand the specimenshaving 13 or 15,often on a single thoseoverlapped by both of their neighbors,the "-" side. No specimenswere observedto have 16 elements,by listingthe positionsof the "+" elements ossicles,a number seen rarely in Gallusgallus separatedby commas,then a semicolon,followed by (Lemmrich 1931). Lemmrich examined only a the positionsof the "-" elementsseparated by com- single cuculiform, Cuculuscanorus, with 12 os- mas. The ossiclesoverlapped by one neighbor and sicles;all 25 cuculid specieswe examinedagreed overlappingthe other ("imbricating" ossicles)are ex- with this finding (Fig. 1E). All musophagids cluded in this notation. In this way, the ring in Fig. examined (Fig. 1F) had 13 ossicles. 1A would be recordedas 1,7;4,9.In Lemmrich's Type Opisthocomus,Cuculiformes, and cracid and B pattern, only a single ventral "+" element and a phasianidGalliformes all characteristicallypos- single dorsal "-" element are present. Hence, the pattern in Fig. lB is designated1;7. sessLemmrich's (1931) Type A patternof ossicle Hypothesesof phylogeneticrelationship were based overlap.The modal ossicledistribution pattern on the tenet that only sharedderived characterscon- in Opisthocomus(Fig. 1A) was 1,7;4,9,although tain useful information aboutrecency of commonan- five other patternswere observed(Table 1). cestry(Hennig 1966).Character polarity was deter- Within Galliformes, three major patterns were January1988] ScleralOssicles of Opisthocomus 31 TABLE1. Numbersand patternsof scleralossicles in representativespecies of Galliformes,Cuculiformes, and Opisthocomus.Pattern designationsare describedin the Methods. Numbers in parenthesesindicate subsamplesize. Modal configurationsfor variable speciesare in boldface. Specimens/rings Taxon examined No. of ossicles Pattern Megapodiidae Aepypodiusarfakianus 1/2 14 1;7 Alectura lathami 1/2 14 1;7 Macrocephalonrnaleo 1/2 14 1;7 Megapodiusfreycinet 6/10 14 1;6 (1) 14 1;7 (9) Cracidae Aburria aburri 2/4 14 1,9;7,10 A. pipile 4/6 14 1,9;7,10 Charnaepetesgoudotii 2/3 14 1,9;7,10 (2) 15 1,9;7,11 (1) Crax daubentoni 1/2 15 1,9;7,10 C. mitu 1/2 14 1,9;7,10 C. pauxi 2/3 14 1,9;7,10 15 1,9;7,10 15 1,10;8,11 C. rubra 2/4 13 1,8;6,9 (2) 14 1,9;7,10 (1) 15 1,9;7,10 (1) Nothocrax urumutum 1/2 14 1,9;7,10 Ortalis canicollis 3/3 14 1,9;7,10 O. cinereiceps 1/2 14 1,9;7,10 O. garrula 1 / 1 14 1,9;7,10 O. motmot 2/4 14 1,9;7,10 O. vetula 3/6 14 1,9;7,10 Penelopealbipennis 1/2 14 1,9;7,10 P. jacquacu 6/10 14 1,9;7,10 P. purpurascens 2/4 14 1,9;7,10 (3) 15 1,9;7,11 (1) Phasi.anidae Meleagridinae Agriocharis ocellata 1/2 14 1,9;6,10 Tetraoninae Bonasa urnbellus 1/2 14 1,9;6,10 Dendragapusobscurus 3/4 14 1,9;6,10 Lagopuslagopus 1/1 14 1,9;7,10 Tympanuchuscupido 1/1 15 1,10;8,11 T. phasianellus 1/2 14 1,9;7,10 15 1,10;8,11 Odontophorinae Colinus cristatus 1/1 14 1,9;6,10 C. virginianus 1/2 14 1,9;6,10 Dactylortyxthoracicus 2/3 14 1,9;6,10 Callipeplacalifornicus 16/29 14 1,8;6,10 (2) 14 1,9;6,10 (23) 14 1,9;6,11 (1) 15 1,9;6,10 (1) 15 1,9;7,11(2) Philortyxfasciatus 1/2 14 1,9;6,10 Phasianinae Perdicini Coturnix coturnix 1/1 14 1,9;6,10 Perdix perdix 1/1 14 1,9;6,10 Phasianini Gallusgallus 1/1 14 1,9;6,10 32 DE QUEIROZ AND GOOD [Auk, Vol. 105 TABLE 1. Continued. Specimens/rings Taxon examined No. of ossicles Pattern G. sonneratii 1/ 1 14 1,9;6,10 Lophuraswinhoei 1/2 14 1,9;6,10 Phasianuscolchicus 1/ 1 14 1,9;6,10 Numidinae Acrylliumvulturinum 4/6 13 1,9;6,10(1) 14 1,9;6,10 (4) 15 1,9;6,11 (1) Gutteraplumifera 3/4 14 1,9;6,10(3) 14 1;10(1) G. pucherani 1/2 14 1,9;6,10 15 1,9;6,10 Numidameleagris 5/9 14 1,9;6,10(8) 14 1,9;7,10 (1) N. mirrata 2/2 14 1,9;6,10 Opisthocomidae Opisthocomushoazin 14/24 11 1,6;4,7(1) 11 1,6;4,8 (3) 11 1,7;4,8 (1) 12 1,7;4,9 (11) 12 1,7;5,9 (1) 13 1,7;4,9 (5) 13 1,8;4,10(2) Musophagidae Corythaeolacristata 2/3 13 1,7;4,9 Corythaixoidesleucogaster 1/2 13 1,6;4,9 13 1,7;4,8 Criniferpiscator 1/2 13 1,7;4,9 14 1,7;4,10 C.
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