The Auk 111(4):873-880, 1994 ONTOGENETIC EVIDENCE FOR RELATIONSHIPS WITHIN THE LARIDAE W. PARKER CANE Departmentof Ornithology,American Museum of NaturalHistory, Central Park West at 79th Street, New York, New York 10024, USA Al•sTP,ACT.--Comparative growth patternsof selectedcranial and postcranialskeletal char- actersare used to test hypothesesof phylogeneticrelationships between the major groups within the family Laridae.The developmentof the bill in skimmersand ternsis characterized by highly nonlinearsize-dependent allometries in contrastto the relativelyconstant, linear allometricrelationship found in gulls. Thesecomparative ontogenetic trajectories thus sup- port the hypothesisthat skimmersand terns are more closelyrelated to one anotherthan either is to the gulls. The linear size-dependentallometry found throughoutdevelopment in gulls is similarto that found early in the ontogenyof all larids.In contrast,the highly nonlinearallometry which characterizesthe later stagesof developmentin ternsand skim- merssuggests additional complexity in the geneticcontrol of bill development.The more parsimoniousphylogenetic hypothesis is that the shapeof the bill in gulls and skuasis the more primitive characterstate. The bill shapein skimmersrelative to terns may reflectthe heterochronicextension of the ontogenetictrajectory characteristic of the later stagesof developmentin terns.Ontogenetic transformations found amongpostcranial characters are consistentwith the hypothesisof relationshipsbased on bill ontogenies.However, because of similar nonlinear characteristicsin both gull and tern growth trajectories,phylogenetic inferencesdrawn from the relativeontogenies of postcranialdimensions are consideredless compelling.Received 22 January1993, accepted 27 March 1993. A 1,4UMI•ERof hypothesesof phylogenetic re- the bill. Here I describethe ontogenetic trans- lationshipsamong the major groupsof birds formationsunderlying these bill-shape differ- comprisingthe Laridae(skuas, gulls, terns,and encesand examinetheir phylogeneticimpli- skimmers)have been suggested(for historical cations. Gulls and terns also can be differentiated summary,see Sibley and Ahlquist 1990). These morphometricallyby several postcranialchar- can be summarized in three phylogenetic trees acters;consequently, the phylogeneticinfer- (Fig. 1). The first hypothesis(Fig. 1A), which ences that can be derived from differences in suggeststhat the ternsand gullsare moreclose- the underlying postcranialdevelopmental tra- ly related than either is to the skuas(Stercora- jectoriesare explored. riinae) and skimmers (Rynchops),reflects the traditional classificationused by Peters (1934) and Wetmore (1960), and is supported by evi- MATERIALS AND METHODS dence from protein electrophoresis(Hackett Specimensin development series.--During the 1988, 1989)and DNA-DNA hybridization (Sibley and 1989, and 1990 breeding seasons,31 Common Tern Ahlquist 1990).Behavioral analyses (Moynihan (Sternahirundo) embryos ranging in agefrom 10 days 1959;see also Burger and Gochfeld 1990) sup- of incubationto 22 days(pipping), and 58 youngfrom port a similar relationship. In contrast,a closer 1 to 57 daysposthatching, were collected or salvaged relationshipbetween the skuasand gulls and on Great Gull Island (GGI). The island, which lies at between the skimmersand terns (Figs. lB and the eastern end of Long Island sound (72ø07'W, 1C) has been suggestedby comparative para- 41ø12'N),Suffolk Co., New York, is the siteof a long- sitology(Timmermann 1957) and an analysisof term study of reproductivesuccess in the Common Tern (Haysand Riseborough1972). Each year a team skeletal morphology (Strauch 1978). checksthe island daily, numbering new nestsand Basedon a morphometricanalysis of skeletal eggs.When chickshatch they are bandedand the characters,Schnell (1970b) felt that, pheneti- nest associationrecorded. Consequently, the age of cally, skimmers showed similarities to terns, chicks later recovered is known to within 24 h. with skimmersand terns being differentiated Forother taxa, developmental specimens consisting from gullsand skuasprimarily by charactersof of 10 Herring Gull (Larusargentatus) and two Great 873 874 w. PARKERCANE [Auk, Vol. 111 A HerringGull A Skuas Skimmers Gulls Terns Common Tern B Skuas Gulls Terns Black Skimmer Skimmers C Skimmers Terns Gulls B -- Skuas HerringGull•=••=•=•• Fig. 1. Three cladogramssummarizing alternative ' ' hypothesesof phylogeneticrelationships within the Laridae. Common Tern Black-backedGull (Larusmarinus) embryos and young were collected near or on Great Gull Island. The Black Skimmer(Rynchops niger) developmental material was obtained from six embryos and juvenile specimens housed in the anatomical collection of the American Museum of Natural History (AMNH). For freshly collected material, embryos were re- moved from the egg and, after removal of the ex- traembryonicmembrane, placed immediately into 10% BlackSkimmer'•'l buffered formalin. Larger specimenswere injected Fig. 2. Bill measurementsused. Bill shapesat about intraperitoneallywith the fixative.After 24 to 48 h time of hatching shown on left, and adults on right. (dependingon size),embryos were transferredto 70% Drawings are not to scale.(A) Upper bills with bars isopropanol.Posthatching specimens were skinned representingthe PRENAR (seeAppendix 2). (B) Man- before being placed in formalin for severaldays to dibles with SYMLEN measure indicated. one week. The few specimensthat showedabnormal osteologicaldevelopment (e.g. cranial deformitiesor abnormalnumbers of digits) have been excludedfrom Tern, one or two specimenswere measured(Appen- the analysis. dix 1). The adult Common Tern data representsthe Specimenswere clearedand stainedusing a mod- averagesof 28 male and 38 female specimens. ification of the Alcian Blue/Trypsin/Alizarin Red S Measurements.--Thebill and postcranialmeasures technique (Wasserzug1976, Dingerkus and Uhler usedare similar to thosedescribed by Schnell (1970a; 1977)in which cartilageis renderedblue and calcified see my Appendix 2 and Fig. 2). The measurements bone red. After staining, specimenswere stored in for the development series encompassboth the os- glycerinwith thymol crystalsadded to inhibit con- sifted and cartilaginousportions of all elements.All tamination. measurementswere madeusing digital calipersunder Adultspecimens.--Adult skeletal measurements were a binocular0.7 to 4.2x dissectingmicroscope equipped obtained from material housed in the anatomical col- with 10 x W.F. eyepieces.Smaller embryos were mea- lections of the AMNH, U.S. National Museum, and sured using a Bauschand Lomb 7.5 x ocular microm- CarnegieMuseum. For taxaother than the Common eter calibrated with a steel rule. October1994] ComparativeLarid Ontogenies 875 T^BLE1. Threeprincipalcomponents extracted from covariancematrix of postcranialskeletal characters ß Gull (seeAppendix 2) for adult larids(taxa in Appendix 4 o Skua 1). [] Tern ß Skimmer Variable P1 P2 P3 COR 0.26 0.15 -0.24 SCP 0.24 0.16 -0.30 ILM 0.26 0.21 0.01 ISH 0.28 0.10 0.04 SAC 0.16 0.44 0.05 FEM 0.29 0.09 -0.07 TBT 0.32 -0.17 0.15 TMT 0.36 -0.52 0.58 TOE 0.33 -0.51 -0.67 10 ' 12' ' 1•4 16 HUM 0.29 0.07 0.09 General Size RAD 0.28 0.19 0.17 CMC 0.26 0.09 0.04 Fig. 3. Logarithmof length of mandibular sym- PRX 0.21 0.29 0.05 physisrelative to generalsize (see text) for gulls,sku- Eigenvalue 1.815 0.046 0.018 as, terns, and skimmers. Solid lines are least-squares Percent trace 95.9 2.5 1.0 fits of data for terns and gulls. shown in Table 1 have been standardized to unit Various models for the use of size- or age-depen- length. Allometric coefficients(b) for the equation dent allometrictransformations in phylogeneticanal- ln(Y) = a + b In(general size) were obtained from ysishave been proposed(Alberch et al. 1979, Kluge bootstrapestimates of the reducedmajor axesfits of and Strauss1985, Kluge 1988).Here the analysisfo- the data using a FORTRAN program. cuseson size-dependentstatic (adult) and ontogenetic allometriesof individual elementsrelative to general RESULTS growth or size. I have defined the "general size" of an individual specimento be equal to the sum of the Schnell (1970a) found the primary variables logarithmicallytransformed values of 13 postcranial discriminating between terns and gulls to be measuresfor that specimenmultiplied by 0.277 (the squareroot of the inverseof the numberof variables). the length of the os premaxillaerostral to the The resultantvalue is then comparableto that which anterior edge of the nasal opening (PRENAR) would be derived from principal-componentsanal- and the length of the dentarysymphysis of the ysis in the caseof purely isometricgrowth. In such mandible (SYMLEN; see Appendix 2). The ex- analyses,the generalsize of a specimenis often con- tent to which these measuresvary acrossthe sidered equivalent to the score of the specimen on Laridaecan be seenin Figure 2. Relative to total the first principal component (PC1). In the caseof bill size, these measures in terns and skimmers isometric growth, PC1, when standardized to unit are quite large, while in gulls and skuasthey length, would have all variable coefficientsequal to are relatively small. Figure 3 shows the inter- p(-0.5)where p is the numberof variables(see Pimentel 1979:58+). Standarization of the componentsto unit specificallometric relationshipsbetween SYM- lengthhas the convenientmathematical property that LEN and general size among the Laridae. The the anglebetween vectors can be calculatedby simple adult larid taxa included in this analysis