Phylogenetic Patterns of Size and Shape of the Nasal Gland Depression in Phalacrocoracidae

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Phylogenetic Patterns of Size and Shape of the Nasal Gland Depression in Phalacrocoracidae PHYLOGENETIC PATTERNS OF SIZE AND SHAPE OF THE NASAL GLAND DEPRESSION IN PHALACROCORACIDAE DOUGLAS SIEGEL-CAUSEY Museumof NaturalHistory and Department of Systematicsand Ecology, University of Kansas, Lawrence, Kansas 66045-2454 USA ABSTRACT.--Nasalglands in Pelecaniformesare situatedwithin the orbit in closelyfitting depressions.Generally, the depressionsare bilobedand small,but in Phalacrocoracidaethey are more diversein shapeand size. Cormorants(Phalacrocoracinae) have small depressions typical of the order; shags(Leucocarboninae) have large, single-lobeddepressions that extend almost the entire length of the frontal. In all PhalacrocoracidaeI examined, shape of the nasalgland depressiondid not vary betweenfreshwater and marine populations.A general linear model detectedstrongly significant effectsof speciesidentity and gender on size of the gland depression.The effectof habitat on size was complexand was detectedonly as a higher-ordereffect. Age had no effecton size or shapeof the nasalgland depression.I believe that habitat and diet are proximateeffects. The ultimate factorthat determinessize and shape of the nasalgland within Phalacrocoracidaeis phylogenetichistory. Received 28 February1989, accepted1 August1989. THE FIRSTinvestigations of the nasal glands mon (e.g.Technau 1936, Zaks and Sokolova1961, of water birds indicated that theseglands were Thomson and Morley 1966), and only a few more developed in species living in marine studies have focused on the cranial structure habitats than in species living in freshwater associatedwith the nasal gland (Marpies 1932; habitats (Heinroth and Heinroth 1927, Marpies Bock 1958, 1963; Staaland 1967; Watson and Di- 1932). Schildmacher (1932), Technau (1936), and voky 1971; Lavery 1972). othersshowed that the degree of development Unlike most other birds, Pelecaniformes have among specieswas associatedwith habitat. Lat- nasal glands situated in depressionsfound in er experimental studies (reviewed by Holmes the anteromedialroof of the orbit (Siegel-Cau- and Phillips 1985) established the role of the sey 1988). In specieswith extra- or supraorbital nasal gland as an extrarenal excretory organ nasal glands, glandular tissue can enlarge by that maintainselectrolyte homeostasis and water growth outward from the skull (Owen and Kear balanceduring conditionsof salt-loading. 1972)and by increasein width (Bock1958), but The size of the nasalgland and its degree of rarely by increase in length (Staaland 1967, function varies alsowithin species.Marine pop- Peaker and Linzell 1975). Becausecranial bone ulations have larger glands and greater func- is membranous, mesenchymal, and nonintus- tional activity than do freshwater populations susceptive,and becauseit grows very slowly of a given species(Schmidt-Nielsen 1959, 1960, if at all after ossification and maturation (de 1965; Peaker and Linzell 1975). Experimental Beer 1937,Bellairs and Jenkin 1960),change in studies with captive wild and domestic birds bony outline of the gland depressionmust oc- indicate that gland size (i.e. mass)and function cur slowly. Thus, functionally inducedgrowth increasedquickly in individuals of somespecies of the nasal gland in the orbit is constrainedin when subjectedto high electrolytestress or low Pelecaniformesbecause substantial thickening water intake (Holmes et al. 1961, Ellis et al. 1963, of the gland without osteologicalaccommoda- Peaker and Linzell 1975). tion could distort the eye. In other species,accommodation to salt-load- I have shown qualitatively (Siegel-Causey ing is less effective (Skadhauge 1981). Devel- 1988) that the size and shape of the nasal gland opment and growth rate in captive Mallards depression is variable within shags and cor- (Anasplatyrhynchos) that were fed 1%solutions morants (Phalacrocoracidae).In this study, I of sodiumchloride were reducedcompared with surveyedthe variation in size and shape of the development and growth of birds fed fresh nasalgland depressionin the orbit of selected water (Schmidt-Nielsen and Kim 1964). Data members of this family. I examined its pre- from field populationsof wild birds are uncom- sumptive associationwith gland size relative to 110 The Auk 107: 110-118. January 1990 January1990] PhalacrocoracidaeNasal Glands 111 Fig. 1. Outlinesof the ventral view of the frontal bone and nasalgland depressionin selectedPelecani- formes.All views representthe area indicated in Figure 2: lower; shadedareas represent the nasal gland depression:(a) GreatFrigatebird; (b) White Pelican;(c) Red-footedBooby; (d) Northern Gannet;(e) Anhinga; (f) Little Pied Cormorant;(g) OlivaceousCormorant (left, freshwater;right, marine); (h) Double-crested Cormorant (left, freshwater;right, marine); (i) Pied Cormorant;(j) Little Black Cormorant;(k) Brandt'sCor- morant;(1) Black-facedCormorant; (m) SocotraShag; (n) CapeShag; (o) Imperial Shag,marine (left, e; right, •); (p) Imperial Shag,freshwater (left, e; right, •); (q) RockShag; (r) PelagicShag; (s) Red-leggedShag. collectionhabitat, age (measuredby size of bur- I measuredcranium length and frontal width by sa of Fabricius),size, and speciesidentity. dial calipersto a 95% replicated accuracy(RA) of 0.1 mm. The least frontal width was the minimum width METHODS measuredon the frontal (Fig. 2: upper). Length and width of the bursa of Fabricius were measured in the All skeletal measurements were done on museum field to nearestmm with dial calipers,but determi- specimens.Scientific names and sample sizes of species nations of RA were not made. usedin this studyare in parentheses:Reed Cormorant I classified collection localities as freshwater and (Microcarboafricanus; 15), Little Pied Cormorant (M. marine (saltwater) habitats; ambiguous caseswere melanoleucos;21), Brandt's Cormorant (Compsohalieus classifiedas missing. Species identity, gender,and age penicillatus;4), Black-facedCormorant (C. fuscescens;were determined at the time of collection or, in the 2), OlivaceousCormorant (Hypoleucus olivaceus; 50), caseof museumspecimens, from the label. Unknown Double-crested Cormorant (H. auritus;57), Little Black genderwas coded as missing. I codedthose specimens Cormorant (H. sulcirostris;3), Pied Cormorant (H. var- without agedeterminations as adults unless there was ius; 4), Great Cormorant (Phalacrocoraxcarbo; 11), So- evidence(e.g. partly ossifiedbone) to indicatejuve- cotra Shag (Leucocarbonigrogularis; 3), Cape Shag (L. nile status. capensis;4), Imperial Shag(Notocarbo atriceps; 12), Ant- I approximatedthe areaof the nasalglands in species arcticShag (N. bransfieldensis;19), Kerguelen Shag(N. with fusedlobes by the productof the greatestlength verrucosus;2), South GeorgianShag (N. georgianus;2), and width of the nasalgland depressionin the cra- Rock Shag(Stictocarbo magellanicus; 73), PelagicShag nium. For specieswith bilobed nasal glands, I used (S. pelagicus;10), and Red-legged Shag (S. gaimardi; the product of the greatestlength of the medial lobe 30). See Siegel-Causey(1988) for details on system- and the greatestcombined width of both lobes.Mea- atics and nomenclature. surements(see Fig. 2: lower) were made by dial cal- For comparativepurposes, depression outlines for ipers(+ 0.2 mm RA). Theseapproximations may over- Great Frigatebird (Fregataminor; 2), American White estimatethe actualarea of the nasalgland depression, Pelican (Pelecanuserythrorhyncos; 4), Red-looted Boo- especiallyin cormorants,which have lessrectangular by (Sulasula; 2), Northern Gannet (Morusbassanus; 2), depressionsthan do shags.All analyseswere done and Anhinga (Anhingaanhinga; 5) are illustrated(Fig. using log-transformeddata. 1). The nasalglands of tropicbirds(Phaethon spp.) do ! performedmultivariate analyses using the BMDP not occur within the orbit and are not illustrated. A statisticalprograms (Dixon [Ed.] 1988). Becauseof the list of specimensand data are available from the au- sensitivity of the analysisof covariance(ANCOVA) thor. program to small samples,I excluded cells with sam- 112 DOUGLAS$IEGEL-CAUSEY [Auk, Vol. 107 sion surfacesof all specimensI examined were composedof smooth, densebone. There was no osteologicalevidence of vascularization or in- complete ossificationas is seen in speciesthat have extra- or supraorbitalglands (e.g. Procel- lariiformes and Charadriiformes). Phalacrocoracidaeare unique within Pele- caniformes and show intrafamiliar variation in depression shape. Four qualitative characters varied within the cormorantsand shags(char- acters 12-15 in Siegel-Causey1988), but only the shape of the lateral edge of the depression Fig. 2. Generalizedphalacrocoracid cranium and showed intraspecificvariation. This feature is gland depression-relatedmeasurements. Upper: dor- sal view (LFW = least frontal width, CL = cranium influenced by the width of the frontal and the length).Lower: ventral view with palatinesremoved length of the cranium (e.g. the lateral curvature (rectanglerepresents view in Figure 1, DW = depres- increases as the least frontal width decreases sion "width," DL = depression"length"). relative to cranium length). This variation in lateral curvature was evident in Double-crested and Olivaceous cormorants collected from dif- ple sizesof <3. I excludedall caseswith missingdata ferent habitats (Fig. 1: g, h), but it was most for the variables under analysis. Equality of slopes pronounced in comparisonsbetween freshwa- (parallelism)of the regressionsof the dependentvari- ables on the covariatecranium length was testedby ter and marine Imperial Shags(Fig. 1: o, p). The ANOVA, and no significant differences (P
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