The Condor90:885-905 0 The CooperOrnithological Society 1988 PHYLOGENY OF THE PHALACROCORACIDAE’ DOUGLAS SIEGEL-CAUSEY Museum of Natural History and Department of Systematicsand Ecology, Universityof Kansas, Lawrence,KS 66045 Abstract. I undertooka phylogeneticanalysis of the Recenttaxa of Phalacrocoracidae usingqualitative osteological characters. The family comprisestwo subfamilies.The Phal- acrocoracinae(cormorants) comprise four generaof all-dark, littorine species:Microcarbo (microcormorants),Compsohalieus (marine cormorants), Hypoleucos (mesocormorants), and Phalacrocorax(macrocormorants). The Leucocarboninae(shags) comprise five generaof variablyplumaged, littorine, and pelagicspecies: Leucocarbo (guano shags), Notocarbo (blue- eyedshags), Nesocarbo (Campbell Island Shag), Euleucocarbo (New Zealandblue-eyed shags), and Stictocarbo(cliff shags).The relationshipof the anhingas(Anhingidae) to the Phalacro- coracidaeremains problematical and unresolved.Additional analyses using cranial or post- cranialcharacters produced comparable results, with the greatestdivergence obtained when only crania were compared.I discussthe nature of homoplasyin the family: cormorants are characterizedby convergences,shags by reversals.Plumage patterns have functional correlates,but phylogenetichistory may be the ultimate factor. Key words: Phalacrocoracidae;Anhingidae; Phalacrocoracinae;Leucocarboninae; cor- morants;phylogenetics; systematics; osteology. INTRODUCTION ment (Sharpe 1899, Peters 193 1, von Boetticher Since the very first attempts to reconstruct the 1937, van Tets 1976, Dorst and Mougin 1979); phylogeny of the Class Aves, there has been little incomplete treatments dealing with regional fau- controversy over which taxa comprised the Phal- nas, selectedspecies groups, or collection hold- acrocoracidae. More pertinent at the time was ings were more common (Ogilvie-Grant 1898; determining the relationships of the family with- Hutton 1903; Hall 1920; Mathews and Iredale in Pelecaniformes, and that of the order to the 1921; Falla 1932, 1937; van Tets 1965). Most rest of birds. The most widely acceptedphylog- recently, Cracraft (1985) investigated the system- eny was by Wetmore (1934) who positioned the atic relationships among Pelecaniformes, and family between the Sulidae and Anhingidae at confirmed the monophyly of the family. the “primitive end’ of the avian phylogeny. Lit- The classification generally followed in the tle effort was expended by systematists before northern hemisphere is of a single genus Phal- or after this to determine relationships within acrocorux (cf. Dorst and Mougin 1979) some- the cormorants. times supplemented by the monotypic genus The Phalacrocoracidaehave been considered Nunnopterum for the Flightless Cormorant ofthe to comprise approximately 30 speciesin one to Galapagos(cf. Sharpe 1899, Witherby et al. 1940). five genera;the most recent treatment recognizes Other taxonomies often remove the microcor- 29 speciesin one genus(Dorst and Mougin 1979). morants (sensu van Tets 1976) from Phalucro- There has been little consensusamong authori- corax into the genus Huliaetor [sic] (cf. Peters ties on the status of certain speciesand higher- 193 1). In the southern hemisphere, Phalucro- order relationships within the family, possibly corax is partitioned further by the use of Leu- because of sporadic and incomplete systematic cocarbo and Stictocarbo for various shagsof the treatments and changing conceptsof speciesand southern oceans (cf. Falla 1932, 1937). genera. Although cormorants are found world- An ancillary (and essentially trivial) issue has wide, and are usually abundant members of the been whether the anhingas (darters) constitute a littorine avifauna, in the past century there have distinct family or are a subfamily of the Phala- been only a few attempts at a family-wide treat- crocoracidae.Peters (193 l), Olson (1985) Beck- er (1986) and others consideredtheir differences to be sufficient for family standing (i.e., Anhing- * Received23 March 1988.Final acceptance7 July idae), while Dorst and Mougin (1979) Cracraft 1988. (1985) and many others found their similarities 18851 886 DOUGLAS SIEGEL-CAUSEY with the Phalacrocoracidae to be great enough cent Phalacrocoracidaeand Anhingidae using 137 to restrict it to a subfamily (i.e., Anhinginae). osteological characters. I present a hypothetical The first worldwide treatment was by Sharpe evolutionary tree for the family, and discussits (1899) who, without indicating methodology or implications for classification, morphological charactersused, placed all forms from the early convergence, and plumage patterns. Miocene to the Recent into Phalacrocorax, re- This article is dedicatedto the memory ofRalph serving separategenera for an Eocene taxon Ac- W. Schreiber, friend and teacher, who encour- tiornis spp., the Galapagos Cormorant (Nannop- aged me early on to study Pelecaniformes, and terum harrisz),and the extinct Pallas’s Cormorant supported my continuing research on cormo- (Pallasicarboperspicillatus).Because he listed the rants with insight and humor. His sudden death latter speciesalso in Phalacrocorax, this gave it diminishes us all. the notable distinction of belonging to two genera simultaneously. METHODS Peters (193 1) followed a traditional linear ar- rangement of species placed into two genera TAXA AND SPECIMENS (Phalacrocorax, Halietor), but without justifi- I studied skeletons of all Recent taxa of Phala- cation or methodology. Von Boetticher (1936) crocoracidae, except for the Indian Cormorant, considered certain aspectsof external morphol- Hypoleucosjiiscicollis, and some of the island ogy (e.g., rectrix number, abdomen color, etc.) forms of Notocarbo atriceps found in Antarctic and biogeography,and clusteredall of the extant waters (e.g., N. a. melanogenis, N. a. purpuras- forms by general similarity into three genera and tens, etc.), of which no specimens are readily 10 subgenera. He later revised this taxonomy available (Wood and Schnell 1986). In taxa (von Boetticher 1937) and altered speciesallo- known to be particularly variable or encom- cations, generic and subgenericnames, and pro- passingmany subspecies,I studied as many forms poseda resolution of the blue-eyed shagcomplex as possible. In all, I examined 226 specimens of (Leucocarbos.1.) of the southern hemisphere. 36 putative species of cormorants, shags, and Systematists studying southern hemisphere anhingas (Table 1). Except for certain New Zea- Phalacrocoracidaehave been facedwith a greater land shags(Nesocarbo campbelli, Euleucocarbo diversity of speciesthan elsewherein the world, chalconotus,E. colensoi,E. onslowi,E. ranfurlyi: and perhaps as a direct result of this, have pro- one skeleton each), three microcormorants @Ii- posed a variety of taxonomies (cf. Mathews and crocarbocoronatus, M. niger, A4. pygmaeus:one Iredale 1913, Falla 1937, and others). Of these, skeleton each), and the extinct Spectacledor Pal- only van Tets ( 1976) consideredall extant species. las’s Cormorant (Compsohalieusperspicillatus: Using similarities in external morphology and unassociated skeletal elements), I examined at behavior, he apportioned all members of this least two specimens of each species. family into two genera (Phalacrocorax, Leuco- carbo) with three subgenera in the former, and ANALYSIS OF CHARACTERS two in the latter genus. I used 137 osteological characters for the phy- Most recently, Dorst and Mougin (1979) fol- logenetic analysis (Appendix 1); less than one- lowing Peters (193 l), lumped all extant species fourth of these have been described or defined into a single genus Phalacrocorax. Assessments previously, but most are illustrated without iden- of possible specific and superspecific affinities tification in referencesaccompanying the char- were given by footnote but without justification. acter descriptions. Where possible, anatomical Neither Dorst and Mougin nor Peters presented descriptions follow Howard (1929) and Owre an explicit phylogeny of the family, but listed (1967); in many cases,however, suitable names speciesin a linear arrangement, “in taxonomic for featurescould not be determined throughthese sequence” (Peters 1931:iv, Mayr and Cottrell sources, and characters were described instead 1979:vi). by appearance or location. In some taxa previ- To date, no attempt has been made to present ously considered to be of subspecificrank (e.g., anything other than a linear arrangement of E. chalconotus, N. bransjieldensis,Stictocarbo speciesand only van Tets (1976) gave distinct featherstoni), I found sufficient diagnostic char- characters to delineate higher-order relation- acters(autapomorphies) to discriminate them as ships. I undertook a phylogenetic analysis of Re- species (see McKitrick and Zink 1988). In the CORMORANT PHYLOGENY 887 FIGURE 1. General tree of the Recent speciesof Phalacrocoracidae(CI = 0.678, length = 227 steps).Character changesare given in the indicated figureswhich follow. Speciesnames in bracketsindicate presumptiveplacement where no specimenswere available for study. case of N. atricepsand albiventer, two taxa cur- these outgroups and the method of Maddison et rently considered specifically distinct, I was un- al. (1984) to construct a hypothetical ancestor to able to discover any diagnostic osteologicalchar- root the evolutionary tree. I found no differences acters. For this analysis, therefore, they were in tree topology of the Phalacrocoracidae using treated together under the senior synonym, atri- actual outgroup taxa or a hypothetical ancestor,