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Variation in Numbers of Scleral Ossicles and Their Phylogenetic Transformations Within the Pelecaniformes

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Variation in Numbers of Scleral Ossicles and Their Phylogenetic Transformations Within the Pelecaniformes VARIATION IN NUMBERS OF SCLERAL OSSICLES AND THEIR PHYLOGENETIC TRANSFORMATIONS WITHIN THE PELECANIFORMES KENNETH I. WARHEIT, • DAVID A, GOOD,2 AND KEVIN DE QUEIROZ2 •Departmentof Paleontology,University of California,Berkeley, California 94720 USA, and 2Departmentof Zoologyand Museum of VertebrateZoology, University of California,Berkeley, California 94720 USA ABSTRACT.--Weexamined scleral rings from 44 speciesof Pelecaniformesand found non- random variation in numbersof scleralossicles among genera, but little or no variability within genera.Phaethon, Fregata, and Pelecanusretain the primitive 15 ossiclesper ring, while the most recent common ancestorof the Sulae (Phalacrocoracidae,Anhinga, and Sulidae) is inferred to have had a derived reduction to 12 or 13 ossicles.Within the Sulidae, Sula (sensu stricto)exhibits further reduction to 10 ossicles.These patterns of ossiclereduction are con- gruentwith both Cracraft'shypothesis of pelecaniformrelationships (1985) and that of Sibley et al. (1988). The presenceof scleral rings in museumspecimens is significantly greater for Phaethonand Fregata,and lessfor Pelecanus,than would be expectedfrom a random distri- bution. We concludethat the scleralring is of potential systematicimportance, and we make recommendationsfor its preservationin museumcollections. Received 11 August1988, accepted 25 January1989. THE scleralring (annulusossicularis sclerae) is to be a retained primitive character.Therefore, a ring of smalloverlapping platelike bones,the any explanationof the ring's function within scleral ossicles (ossiculasclerae), found within birds must also consider its widespread occur- the sclerain the cornealhemisphere of the eye rence in Vertebrata. Whatever function the betweenthe retinal margin and the conjuncti- scleralring may serve,the number of ossicles val ring (Edinger1929, Martin 1985).The func- per ring varies in a nonrandom pattern among tion of the scleralring as a whole, and the in- some avian taxa (Lemmrich 1931, Curtis and dividualossicles in particular,is poorlyknown. Miller 1938, de Queiroz and Good 1988). Two functions are most often proposedfor the The use of the scleral ring as a systematic scleralring: first, as supportand protectionof character in birds has been limited. Studies have the eye in the region where it is found; alter- been descriptivesurveys, conducted primarily natively, as an attachmentfor the ciliary mus- at the ordinal or familial levels, on ring mor- cles,specifically, the anteriorcorneal muscle (m. phology, function, and variation in ossicle cornealisanterior), which suggestsa role in cor- number and position (e.g. Lemmrich 1931,Cur- nealaccommodation (Lemmrich 1931, King and tis and Miller 1938).While conductingtwo in- McLelland 1984, Martin 1985). Curtis and Mil- dependentresearch projects, one on the scleral ler (1938)also suggested that eccentricityof the ossiclesand phylogeneticrelationships of the ring aperture may facilitate binocular vision. Hoatzin (de Queiroz and Good 1988), and the The arrangementof the ossiclesthemselves is otheron the phylogeneticrelationships within even more problematic, although Lemmrich the Sulidae (Olson and Warheit 1988, Warheit (1931)proposed that having a scleralring com- in prep.), we discoveredwhat appearsto be posedof overlappingplates permits growth of phylogeneticallyinformative patterns of vari- the ring during ontogeny.Lemmrich also pro- ation in numbersof scleralossicles among the posed that the differences in ossicle number pelecaniformgenera. among taxa may be attributed to "growth or- We summarized the numbers of scleral ossi- ganization" (Organisationmerkmal)particular to cles for extant speciesof Pelecaniformes,and taxa. Becausethe scleral ring existsin a wide examinedthese patterns in the contextof cur- variety of vertebrates(Edinger 1929) including rent hypothesesabout pelecaniform relation- nonavian dinosaurs (references in de Queiroz ships.As a result of our survey,we alsofound and Good 1988), its presencein birds appears that scleral rings are not satisfactorilymain- 383 The Auk 106:383-388. July 1989 384 WARHEIT,GOOD, AND DE QUEIROZ [Auk,Vol. 106 tained in osteologicalcollections, and are ab- acrocorax(sensu lato; see below), however, we sent even in some specimensthat are consid- found 14 specieswith a modal number of 13 ered "complete." Accordingly, we make ossicles,4 specieswith 12 ossicles,and 3 species recommendationsfor the preparation of scleral with 12 or 13 ossicles (the modal number of rings in osteologicalspecimens. ossicles could not be resolved for the latter 3 speciesbecause of small samplesizes). Similar- MATERIALS AND METHODS ly, modal numbers of ossiclesvary among the specieswithin the single sulid genus(Sula) rec- We sampled 695 skeletonsfrom 51 speciesof pele- ognizedmost recently by Nelson (1978)and the caniforms. The number of specimenssampled for a American Ornithologists'Union (A.O.U. 1983), particular specieswas determined by its availability in the collections.For specieswith a limited number but doesnot vary within eachof the three sulid of skeletons,all specimenswere examined. If the sam- generarecognized by Olson and Warheit (1988). pie size for a specieswas large (n > 20), skeletons Availabilityof scleralrings.--Availability of were chosenrandomly, but with an effort to maintain scleral rings was not distributed randomly equal numbers of males and females. among the genera (X2 = 42.8, P < 0.001; Table We recordedthe number of completerings present 1); however, an analysisof the residualsof the (0, 1, or 2) for each specimen.When ossicleoverlap Chi-square(see Haberman 1973)shows that not is extreme, some plates may be visible on only one all genera deviate significantlyfrom indepen- side of the ring. Therefore, the number of ossicles dence.The number of scleralrings presentfor that constitute a ring was determined by counting both Phaethonand Fregata are significantly plates on both the inner and outer sides.For speci- greater (X2 = 14.83,SR (standarizedresidual ad- mens with two rings, both rings were examined. In most cases (87%) the number of ossicles in the left justedby estimateof variance) = 1.76,P < 0.05; and right rings was the same, but occasionallythe X2 = 27.54, SR = 2.13, P < 0.05; respectively), number differed (see Curtis and Miller 1938 for uni- while the number of rings presentfor Pelecanus variate statisticsand discussionof constancyof scleral is significantly less (X2 = 37.28, SR = -1.78, P ossiclenumbers between right and left eyes for var- < 0.05) than expected from a random distri- ious taxa of birds). bution. The number of scleralrings present in Mean counts were recorded for those specimens the other genera was not significantly different with both left and right rings preserved.For example, from a random distribution (P > 0.05). The if the number of ossiclesin the left ring was 14 and probabilitiesassociated with the numberof rings the right ring was 15, a count of 14.5 was used for that specimen.This was donebecause using the total absent were not significant (P > 0.05) for all number of scleralrings to calculatethe mode, rather genera,but Phaethon,Fregata, and Pelecanusap- than the preferred total number of specimens,would proachedsignificance (P = 0.10), with Phaethon not only violate the assumptionof independent sam- and Fregatahaving fewer rings absent,and Pele- pies,but would alsobias the mode towardsspecimens canushaving more rings absent than expected. with two rings over those with only one ring. We summarizedthe data in two ways. First, modal DISCUSSION numbersof ossidesare reported for 44 of the 51 species surveyed(no scleralrings were availablefor 7 species). Second,the availability of ossiclesfor each species Basedon comparisonswith ratites, tinamous, was determinedby comparingthe number of speci- and nonavian dinosaurs (de Queiroz and Good mens containingossicles (either one or two) to the 1988), the primitive number of scleral ossicles total numberof specimensexamined. Specimens with for neognathbirds appears to be 14 or 15. Num- broken or disarticulatedrings were excluded. bersin this range are taxonomicallywidespread within Neognathae (Lemmrich 1931,Curtis and RESULTS Miller 1938, de Queiroz and Good 1988). Cra- craft (1985) argued that the pelecaniformsare Variationin thenumber of scleralossicles.--The monophyletic and suggestedthat the Procel- modal numbersof ossiclesper scleralring for 44 lariiformes, Sphenisciformes,and Gaviiformes speciesof pelecaniformsare listed in Table 1. are the most significant outgroups. These out- Ossiclenumbers are distributed in a phyloge- group taxapossess either 14 or 15 scleralossicles neticallyinformative pattern within and among (Lemmrich 1931,Curtis and Miller 1938).Sibley pelecaniformgenera. Within generathere is lit- et al. (1988) suggestedthat the Falconiformes tle variability in ossiclenumber. Within Phal- and Charadriiformesare the closestoutgroups July1989] PelecaniformScleral Ossicles 385 TABLE1. Total number of specimensexamined, number (and percentage)of specimenswith ossicles,and modal number of ossiclesfor speciesof Pelecaniformes.Data associatedwith each genusheading equals the totalsfor all the specieswithin that genus. Specimens Specimens Total No. with Modal Total No. with Modal Taxon no. ossicles(%) no. Taxon no. ossicles(%) no. PHAETHONTIDAE P. harrisi 8 2 (25) 13 Phaethon 35 24(69) 15 P.magellanicus 9 5 (56) 12 P. aethereus 4 2 (50) 14-15 P.melanoleucos 13 2 (15) 12-13 P.lepturus 8 5 (63) 15 P.neglectus 8 8 (100) 13 P. rubricauda 23 17(74) 15 P. olivaceus
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