MONOPHYLY OF THE PASSERIFORMES: TEST OF A PHYLOGENETIC HYPOTHESIS
ROBERTJ. RAIKOW Departmentof BiologicalSciences, University of Pittsburgh, Pittsburgh,Pennsylvania •5260 USA
ABSTR•CT.--Theorder Passeriformeswas largely defined by 19th century anatomistson the basis of pheneticsimilarities. The purposeof this study was to determinewhether the group is monophyleticin the strictcontemporary sense. Similarities used by previouswork- ers were reanalyzedto determine whether or not they could be shown to be derived character statescorroborating the hypothesisof passeriformmonophyly. Of 18 traditional taxonomic charactersanalyzed, none refuted the hypothesisof passeriformmonophyly, 13 failed to corroboratethe hypothesis,and 5 did corroborateit. Theseare the aegithognathouspalate, the "passerine"tensor propatagialis brevis, the bundled spermatozoawith coiledhead and large acrosome,the enlargedhallux, and the type VII deep plantar tendons. To this analysis is added new information from the hind limb musculature. Previous knowledge of oscine musculatureis augmentedby new information from representative suboscines.The division of M. pubo-ischio-femoralisinto Parscranialis and Pars caudalis is confirmedfor suboscines,distinguishing the entire orderPasseriformes from nonpasser- ine birds. In the foot, the lossof a set of intrinsic musclesof the forward digits, previously known from oscines,is also confirmedfor suboscines.These limb-musclecharacters sup- plement the analysisof traditional charactersin corroboratingthe hypothesisthat the order Passeriformesis monophyletic. A functionalanalysis of the passerinefoot showsthat it is a derivedmechanism specialized for perching, but with a reduction in the subtletyand variety of certainother movements. Received9 March 1981, accepted3 August1981.
I• this paper I address the question of fined that it is desirable now to reconsider the whether or not the avian order Passeriformes nature of the largestorder of living birds. is monophyletic,using the conceptof mono- Eldredge and Cracraft(1980: 158) have noted phyly in its strict contemporarysense. I would that a recurrent theme in the history of classi- define as monophyletica group whose char- fication has been the elimination of nonmono- acteristicssupport most stronglythe hypothe- phyletic taxa. The fact that such apparently sis that it consists of all the known descendents nonmonophyleticgroups as "Pisces,""Reptil- of a single commonancestor, that is, a group ia," and "Carduelinae" have long persistedin all of whose members share a more recent com- classifications warns us not to assume that a mon ancestor with each other than with any group is monophyleticjust becauseit has tra- other taxa. In other words, the question is ditionally been formally classifiedas a taxon. whether the order Passeriformes is a clade. In our previous studies of the appendicular There are four reasonswhy this question is muscles,my studentsand I have questioned important in the contextof my research.First, the monophyly of various traditional groups passeriformmonophyly has long been a tacit and have found that suchhypotheses are sup- assumptionbased on a century-olddefinition ported to different degrees.The family Drep- of the assemblageas being "natural" or mono- anididae is hardly definableas monophyletic phyletic in an old and vague senseat best. It except by a geographic argument (Raikow is a phenetic cluster of groups traditionally 1977b, 1978). Monophyly of the ploceid/estril- united by various "similarities" without con- did complex remains uncertain, because no sideration of the nature of those similarities or synapomorphieswere found in the limb mus- of the sorts of information that different kinds cles to reinforce previous arguments (Bentz of similarity can or cannotprovide about phy- 1979). The shrikes (Laniidae) are only weakly logenetic relationships. In recent years our defined as monophyletic(Raikow et al. 1980). conceptsof monophyly and our methods of Some support for monophyly of the Coracii- character analysis have been sufficiently re- formes was found (Maurer and Raikow 1981), 431 The Auk 99: 431-445.July 1982 432 ROBER?J. R^IKOW [Auk, Vol. 99 but it is not unequivocal.On the other hand, similarities will support such a hypothesis. Mono- monophyly of the Piciformesis strongly cor- phyly can be shown by the possessionof characters roborated (Swierczewski and Raikow 1981), as that are best interpretedas being derived at the level is that of the New World nine-primaried oscine of the group in question.I looked for such synapo- assemblagewhen the Vireonidaeare excluded morphies in two places: (1) traditional taxonomic characters from the literature and (2) new informa- (Raikow1978). The evidenceis likewise strong tion from my dissectionsof the limb muscles. that the Atrichornithidae and Menuridae form I reexaminedthe pheneticsimilarities used by pre- a clade (Raikow MS). vious workers as evidencesfor grouping. Such sim- A secondreason for reexaminingpasseri- ilarities could be sharedprimitive characters(sym- form monophyly is that Feduccia(1975, 1977) plesiomorphies), or they could be derived states recentlyproposed that the suboscinesand os- shared with nonpasserinesand not demonstrableas cinestogether do not form a clade,but that the having evolved independentlyin passefines.Such suboscinesare insteadpart of a cladewith sev- characterswould not corroborate a hypothesis of eral coraciiform families, which he termed the monophyly. Alternatively, traditional characters Alcediniformes. This conclusion followed from found to be mostreasonably interpreted as uniquely or independently derived by the Passeriformes a studyof the stapesor middle ear ossicle.Fed- would indicate monophyly. In addition, I searched uccia argued that oscineshave a primitive for new synapomorphiesin the structureof the limb stapes, while suboscinesand Alcediniformes muscles. Most of the literature on avian limb muscles share a distinctive derived condition. Later dealseither with oscinesor with nonpasserines,and Feduccia(1979) recanted this heresyand decid- little work has previouslybeen done on the muscles ed that the suboscines and Alcediniformes do of suboscines.To date I have completedonly a lim- not form the clade originally postulated,but ited survey of suboscinemuscles, but it includesrep- evolved their derived stapes independently. resentativesof all the subordersand major families, Feduccia (1979) also provided evidence from and is adequate for the purposesof this paper. Fol- spermatozoanmorphology that supportsthe lowing the classificationof Wetmore (1960), the sub- oscine speciesdissected include the following: Sub- idea of passeriformmonophyly. Nevertheless, order EURYLAIMh Calyptomena viridis inasmuchas Feducciadid raise a seriousques- (Eurylaimidae);Suborder TYRANNI: Dendrocolaptes tion about passerinemonophyly, and because certhia (Dendrocolaptidae); Certhiaxis cinnamomea his hypothesis and its subsequentretraction (Fumariidae); Thamnophilusdoliatus (Formicariidae); were basedon a limited rangeof data, the mat- Acropternisorthonyx (Rhinocryptidae); Procnias nu- ter remains worthy of reconsideration. dicollis(Cotingidae); Pipra erythrocephala (Pipridae); Third, the long-termgoal of my researchis Tyrannus tyrannus, Pachyramphusrufus (Tyranni- to work out the phylogenetic relationships dae); Pitta guajana (Pittidae); Suborder MENURAE: among passerinebirds, using a cladisticanal- Menura novaehollandiae (Menuridae); Atrichornis ysis mostly of the limb musclesas the method. clamosus(Atrichomithidae). Comparative data on oscines and nonpasserines Beforeundertaking such an analysis,I consider from our laboratory include numerous families as it prudent to determine with reasonablecon- reportedin the following works: Raikow 1973, 1975, fidence that the order is monophyletic, be- 1976, 1977a, 1977b, 1978; Bentz 1976, 1979; Maurer cause,if it is not, then any hypothesisabout 1977; Swierczewski 1977; Raikow et al. 1979; Raikow its genealogywill be wrong. et al. 1980; Swierczewski and Raikow 1981; Berman Fourth, there is a practicalproblem related and Raikow 1981; Borecky1977, 1978; Maurer and to the previous point. In analyzing cladistic Raikow 1981.Additional avian myologicaldata were relationshipsamong passerines,I expectto do taken from the summariesby Hudson (1937) and outgroupcomparisons between passerines and Georgeand Berger(1966). nonpasserinesin order to clusterclades within the Passeriformes.The logical validity of this OUTGROUP COMPARISON procedurerequires that the monophyly of the The traditional taxon Passeriformesis a phenetic order be establishedbefore attempts are made cluster.In order to demonstratethat it is monophy- to determine the polarity of charactertransfor- letic, we must show that its members possesschar- mations within the order (see below). acter states that are derived within the classof birds, that is, conditions for which nonpasserinebirds are METHODS primitive. This requires a method for determining the polarity (primitive-derived directionality) of the In orderto demonstratepasseriform monophyly it charactersin question.The most widely used meth- is not enoughjust to list similarities,because not all od of characteranalysis is the outgroupcomparison. JuLY1982] PasseriformMonophyIy 433
Often in papersin which this methodis used, it is that the ancestralspecies giving rise to the members cited without an adequateexplanation of how it of this genushad the primitive state,and that the works.Perhaps the mostdetailed explanations of the circular nonsetosecondition arose within a lineage methodare given by Ross(1974: 152) who callsit of this group. It is not uncommonfor a writer to "ex-group comparison,"Eldredge and Cracraft assumethat a familiar taxon is monophyletic,but (1980:26, 63), and Watrous and Wheeler (1981). one of the points of this paper is that suchassump- As usuallyexplained, outgroup comparison works tions should not be made. as follows. If a certain character shows variations amongthe membersof a groupof organisms(which MONOPHYLY OF AVES will be calledthe ingroup),and if one of thesevari- In order to demonstratepasseriform mono- ationsalso occurs in otherorganisms (the outgroup), then the variant that occursonly within the ingroup phylywe requirederived states that define the is considereda derived statein that group, the other order as a clade within somelarger group, of being primitive within the group. Here is an ex- which the practicalchoice is the classAves. As ample. Some Hawaiian honeycreepers(Drepanidi- discussedabove, this requires that Aves be dae) have a particulartype of tubular tongue (used consideredmonophyletic, so that the appro- for nectar-feeding),while othershave a simple non- priate outgroupcomparisons can be made. We tubular tongue. Which is the derived condition in must thereforeargue for the monophylyof the family? If we look at the other New World nine- Aves, but to do this by an outgroup compari- primariedoscines we seethat sucha tubular tongue son would require the prior assumptionthat is never present.Therefore, we may concludethat in some still larger group, e.g. the amniotes, is the Drepanididae a nontubular tongue is primitive and a tubulartongue is derived.We may furthercon- monophyletic.That would also have to be cludethat the specieshaving the tubular tongueform demonstrated,requiring yet anotherhypoth- a monophyleticsubgroup of the Drepanididae (Rai- esis, suchas the monophylyof the tetrapods. kow 1977b, 1978). This series of dilemmas is not infinite; even- There is a potential problem with this analysis, tuallyone comesto a hypothesisof the mono- however. As given above, it containsthe unstated phyly of all life, and then thereis no outgroup. assumptionthat the Hawaiian honeycreepersthem- The solutionto this problemis to usea method selvesare a monophyleticgroup, being more closely other than outgroup comparison to demon- related to each other genealogicallythan to any of stratethe monophylyof somegroup so that the the other New World nine-primaried oscines.This study can begin. Gaffney (1979:95) suggests assumptionis necessaryfor the outgroup compari- sonto be logicallyvalid, becausecharacter variations that "... in practiceone usuallyassumes the arise through the processof evolutionarychange in correctnessof a higher-level(more inclusiveor an evolving lineage; there is a temporal polarity to more general)hypothesis and makescompar- the process.If we say that some Hawaiian honey- isons within it." In the present case,I believe creepershave the primitive conditionand othersthe that one can do better than this and provide an derived condition, we mean that the character independentargument for the monophylyof underwenta changein one lineage and that all of Aves. Then, it will be possibleto do valid out- the tubular-tonguedspecies are descendedfrom the group comparisonsbetween Aves and non- ancestralform that first had this changedcharacter. Aves in order to testthe monophylyof the Pas- All of this requires the existenceof a monophyletic seriformes within Aves, which is the real group of specieswithin which this charactertrans- formation took place in one lineage. If we do not purposeof this exercise. have reason to believe that the Hawaiian honey- Here is an argument, not based on an out- creepersform a monophyleticgroup, then we cannot group comparison, that the class Aves is logicallymake a comparisonbetween this group and monophyletic.Feathers are consideredto be an outgroup, becausewe do not know that some homologouswith reptilian epidermal scales Hawaiian honeycreepersare not members of that based on their similar compositionof keratin- outgroup. ized epidermaltissues and their similar devel- Explanationsof the outgroup comparisondo not opment through the interaction of the ecto- always mention this point. For example Ross (1974: derm with a dermal papilla. Epidermal scales 153)illustrates the procedureby describingtwo vari- ations in the form of the male genitalia of the leaf- occurthroughout the "reptilia," whichpredate hopper genus ExitJanus:triangular with setae or birds in the fossilrecord. Epidermal scalesare circularwithout setae.In related genera the form is themselvesregarded as a derived specializa- triangularwith setae.Ross concludes that the trian- tion of the stratum corneum, a universal tet- gular, setosecondition is primitive. Here, the un- rapod characterfirst appearingin the "am- statedassumption is that Exitianusis monophyletic, phibia," which appearin the fossilrecord even 434 ROBERTJ. RAIKOW [Auk, Vol. 99 earlier. Not only are feathersclearly derived in which of these charactersmay be considered vertebrates, but they are no doubt uniquely to be derived at the level of the Passeriformes derived. The structuralcomplexity of feathers, and which will, therefore, corroborate the hy- and their severaldiverse but often intergrading pothesis of passeriformmonophyly. types, makes it appear highly unlikely that The analysiswas performedby asking a se- they evolved more than once. ries of questionsabout each character,as out- Similar argumentsmay be made regarding lined in Fig. 1. First, is the charactervalid or other avian characters,such as the specializa- invalid; that is, was the character described tion of the forelimb as a wing. This involves correctly in the first place?If not valid, I re- a complex of lossesand fusions of elements, jected it as possibleevidence for passeriform which first appear separatelyin the embryo, to monophyly. The validity of most characters producethe specializedstructure of the wrist was not checked by reexamination of speci- and hand. Likewise derived is the avian fore- mens, so in generalvalidity was assumed,and limb musculature, with its enormously en- the analysis began with the secondquestion: larged wing depressorM. pectoralisand the Is the characterprimitive or derivedwithin Aves? elevator M. supracoracoideus,situated ventral If primitive within Aves, a charactercannot be to the wing but insertingdorsally via the pul- derived for passeriformsand was rejected.If ley provided by the foramen triosseum.The the question could not be answered, then the evolution of this flight mechanismfrom the characterwas also rejected,as it is preferable reptilian condition via an intermediate stage to reject potentially corroborative evidence in Archaeopteryxhas been described by Os- than to chanceaccepting false evidence. If the from (1976a). character is derived within Aves, the next Again, the respiratorysystem, with its com- question is whether it is unique to Passeri- plicated system of air sacsand its unique or- formes.If it is, then it stronglycorroborates the ganization of air capillaries,is seen to be de- hypothesisof monophyly.If it is derivedwith- rived in birds throughits functionalcorrelation in Aves but is not unique to Passeriformes, with flight and endothermy,which are also there are two possibleexplanations: it may or derived in comparison with more ancient tet- may not have been independently evolved in rapod groups. the Passeriformes.If it was not independently The preceding argument for avian mono- evolvedby the Passeriformes,then it is a de- phyly is based on the temporal(stratigraphic) rived state shared by the passerinesand some sequenceof fossil vertebratescorrelated with other group(s),was presumablypresent in the the distribution of characters associated with common ancestor of the passerines and those the evolution of adaptive specializations,some other groups, and cannot be used to argue aspectsalso being corroboratedby embryolog- monophyly of the Passeriformes.On the other ical information. Any of these features alone hand, if the state is derived within Aves, is not is convincing evidence of avian monophyly; unique to passerines, but is independently their co-occurrence in birds reinforces the ar- evolvedin Passeriformesfrom its origin in other gument. groups (convergenceor parallelism),then it does support passerinemonophyly. Again, if the question could not be decided, then the ANALYSIS OF TRADITIONAL CHARACTERS characterwas rejectedso as to avoid the chance The characters on which the order Passeri- of error. formesis basedare mostlyanatomical features The most convincingargument for mono- discoveredduring the nineteenth century and phyly would be given by charactersthat are summarized by Beddard (1898) and Ridgway derived within Aves and unique to Passeri- (1901), though some were describedmore re- formes. Characters derived within Aves, not cently. The number and diversity of these unique to Passeriformes,but thought to have characterssuggests at first glancethat the order been independently evolved by them are Passeriformesis firmly establishedby a thor- somewhat less certain, because they require ough technicaldiagnosis. As presented,how- one more decisionin their analysisand hence ever, these are pheneticcharacters, similarities involve one more potential sourceof error. recorded without consideration of their nature. In the following analysisthe polarity of some The purposeof the following analysisis to see traditional characterswill be tested by out- 1982] PasseriformMonophyly 435
CHARACTER -• INVALID
VA LID -'"' PRIMITIVE IN AVES
NOT INDEPENDENTLY DERIVED NOT UNIQUE IN = • EVOLVED IN IN AVES PASSER FORMES PASSERIFORMES
UNIQUE IN INDEPENDENTLY EVOLVED PASSERIFORMES IN PASSERIFORMES
Fig. 1. A schemefor determiningwhether traditional phenetic characters are derivedwithin Aves at the level of Passeriformesand whether they will thereforecorroborate the hypothesisof passeriformmonophyly. Charactersthat are accepteddo corroboratethe hypothesis; those that are rejecteddo not. See text for dis- cussion. group comparisonswith "reptiles" on the as- and McEvey (1969:205) point out that Huxley sumption, discussedabove, that the classAves (1867)used a complexof charactersin defining is monophyletic. In the case of charactersfor his palataltypes but that more recentworkers which such comparisonscannot be made be- often simplified the definitions, with a result- cause they occur only among birds, other ing loss of precision.On the basis of the full methods of analysis will be used where pos- set of characters, these authors determined that sible. the palatein the Pedionomidaeand Turnicidae (1) Palate aegithognathous.--Huxley(1867) is schizognathousand not aegithognathous,as defined several palatal types on the arrange- is sometimesstated (e.g. Beddard1898: 321). ment of the bones. I examined the descriptions In the Capitonidae (Piciformes), the skull is and illustrations of the palate in archosaurs "aegithognathouswith a desmognathousten- given by Romer (1956, 1966). Often the palate dency" (Beddard1898: 195), meaning that the is poorly known, but it appearsclear that ae- maxillopalatinesmay blend with the nasalsep- githognathismis not presentin the Thecodon- tum or with each other across the midline. The tia, Crocodilia, Saurischia, Ornithischia, or vomer is truncated caudal to the line of the Pterosauria.Generally, the vomers, if known, palatines, instead of rostral to it as in passer- are paired and do not show the characteristic ines (Beddard 1898: 196). There are other dif- form of aegithognathousbirds. In addition, the ferences. Collectively, these suggestthat the maxillopalatinesare lacking, unlessMcDowell capitonidcondition is not directlycomparable (1978) is correct in his assumption that the to the passerine condition. Also among Pici- avian maxillopalatinesare homologouswith formes, Indicator is reported as being aegith- the reptilian palatines, in which case they are ognathous(Beddard 1898: 197). Swierczewski still dissimilar. I concludethat the aegithog- and Raikow (1981) studied the limb muscula- nathous palate is a derived condition within ture of the Piciformes and found that the Cap- Aves. itonidae are a fairly derived family within the It is not unique to passerines,however. Bock order and that the Indicatoridae are even more 436 ROBERTJ. RAIKOW [Auk, Vol. 99 highly derived. Synapomorphyof the ques- coraciiforms (Beddard 1898). There is no indi- tionable piciform aegithognathism with the cation in the literature that the passerine con- passerine condition would involve extensive dition is in any way distinctive; hence, this con,flicts with myologicalfeatures that clearly character will not corroborate the hypothesis place both barbets and honeyguides in the of passeriformmonophyly. monophyleticorder Piciformes. (3) Only left carotid artery present.--Both The swifts (Apodidae) also have an aegith- Beddard (1898) and Ridgway (1901) cite the ognathouspalate. Beddard (1898: 229) notes presenceof only the left carotidartery as a pas- that, while in passerinesthe vomer is truncat- serine character.More recently, Glenny (1955) ed in front of a line joining the maxillopala- studied the patternsof avian carotidarteries in tines, in swifts this truncation is at the level of some detail. He proposed that the primitive this line, though the significanceof this dif- condition in birds is the presenceof both left ferenceis obscure.At the turn of the century and right arteries and that various patterns of the closerelationship of the swifts to the pas- reduction and losscould be recognized,which serine swallows (Hirundinidae) was hotly de- he identified by a coding system."All birds, bated, but their similarities have now been insofar as presently known, develop a com- dismissed as convergenceassociated with ae- plete aortic arch system, and this system rial insecthawking. Beddard(1898: 224) points undergoesa seriesof developmental(atrophic) out many differencesbetween swifts and pas- deletions and other modifications which result serines, including several in the limb muscu- in the adult arterial arrangement-patterns lature that seem highly significant to me, as ..." (Glenny 1955: 609). In current terms, they depart greatly from the usual passerine Glenny proposes that loss patterns are derived conditions. Sibley and Ahlquist (1972: 198) re- states, as indicated by a developmental crite- view the problem thoroughly. Although a con- rion. Passeriforms share a derived arterial con- nection to the Passeriformesis possible, the dition, termed B-4-s by Glenny, but this also questionof the swifts' relationshipsto the Tro- occursin most piciforms,in trogons,in colies, chilidae, Caprimulgiformes,Coliiformes, and and in several other orders and families of Trogonidae appears at least as important. I birds. Thus, the characteristic is derived in agree with Sibley and Ahlquist (1972: 206) that passerinesbut is far from unique. There is no this problem is one of the most interestingin apparent method to determine whether it is nonpasserine systematics. Meanwhile, how- autapomorphicfor the Passeriformesor shared ever, I see little evidence that the swifts are with other groups. Therefore, this traditional particularly close to the passerinesand think charactercannot corroboratethe hypothesisof it more likely that their palatal similarities are passeriformmonophyly. due to convergencethan to immediate com- (4) Oil glandnude.--In somebirds, the orifice mon ancestry. of the uropygial gland is surroundedby a circle In general, then, the aegithognathouspalate of feathersforming a tuft that actslike a wick; appears to be a character of some structural this condition is called tufted. In others, in- complexity that is probably independently de- cluding passerines, the circlet is lacking, giv- rived in the Passeriformes and therefore cor- ing the nude condition. Both conditions are so roborates the hypothesis that the order is wide-spread among birds that the character monophyletic. cannot be shown to be derived for the Passer- (2) Atlas perforated.--The atlas and axis are iformes and therefore does not corroborate the the first two cervical vertebrae. The atlas artic- hypothesisof passerinemonophyly. ulates within the odontoid processof the axis. (5) Wing eutaxic.--In many birds there is a The opening in the atlas into which the odon- gap in the row of secondaryremiges, the fifth toid processfits may be fully enclosed(perfo- secondaryappearing to be absent while its rated atlas), or it may be open dorsally covert remains in place. The condition in (notched atlas). It is perforated in the Passeri- which the gap occursis calleddiastataxy, while formes. I cannotdetermine the polarity of this that in which the gap is absentis calledeutaxy. character,but it does not matter. If primitive, Passeriformes are eutaxic. I cannot determine it is of no value. If derived, it is far from unique the polarity of this characterby outgroupcom- in the Passeriformes,being present in various parison, because "reptiles" lack feathers, so other groups, including many piciforms and both possibilitiesmust be considered.If it is JvLY1982] PasseriformMonophyly 437 primitive within Aves, then it is not derived Maurer 1977 mentions it). It is also lacking in for the Passeriformes.If it is derived, however, at leastsome piciforms and in hummingbirds, it is not unique to Passeriformes;on the con- swifts, owls, parrots, cuckoos, turacos, and trary, there are many groupsthat show each some caprimulgiformes(Beddard 1898). It is condition, and occasionallyboth conditions thereforeunnecessary to worry about the po- occur in a single order or family. Becauseof larity of this character;the absenceof the bi- this widespreadoccurrence of both conditions, ceps slip is so widespread that it cannot be I can see no basisfor suggestingthat the eu- proposed as a uniquely derived state of the taxic condition in passerines, even if derived, Passeriformes. was derived independentlyfrom its origin in (9) Tensorpropatagialis brevis tendon "passer- any other eutaxicgroups. Therefore, the con- ine".--This muscle arises in the shoulder and dition of eutaxicfeatbering cannot be used as sendsits tendon through the patagium to an evidence for monophyly of the order Passeri- insertion on the surface of the extensor meta- formes. carpi radialis, a forearm muscle. The tendon (6) Intestinalceca srnall.--Beddard (1898) and doesnot end there, however.After makingits Ridgway (1901) both report that the intestinal attachment,it turnsproximad and passesto an cecaare small in passerines.This characterap- insertion on the humerus. Garrod (1876) con- pearsto be of no value; "The caecaare among sideredthis to be a goodcharacter for defining the most variable organsof birds" (Beddard the passerinebirds. The condition as described 1898:30). Van Tyne and Berger(1976: 576) also does appear to be characteristicof passerines discuss this character. The ceca are often ves- generally, including suboscines,though Gar- tigial as in the Passeriformesand may vary rod did note some minor variations, as I have considerablyin closelyrelated birds with dif- also.These seem insignificant, however, com- ferent feeding habits. Small.ceca are not pared to the great diversity that the muscle unique to the Passeriformes,nor is there a ba- showsin other groups.It is not possibleto do sis for determining the polarity of this char- outgroup comparisonswith "reptiles" in ana- acter; hence, it cannot be cited as evidence of lyzing this character,as it is an avian special- passeriformmonophyly. ization associatedwith the patagium of the (7) Expansorsecundariorurn lacking.--Both wing. Becausethis condition appears to be Beddard (1898) and Ridgway (1901) state that unique to the Passeriformes,it is temptingto this small forelimb muscleis absentin passer- suggestthat, if the Passeriformesare shownto ine birds. Berger (1956)reported it in 23 fam- be monophyleticby other characters,then by ilies of both oscineand suboscinepasserines, correlationthis characteris also presumably however, including the Eurylaimidae,Furna- derived at the level of the order. Then to use riidae, Formicariidae,Cotingidae, and Tyran- this as an evidenceof passerinemonophyly, nidae among the latter. Bergeralso referedto however,verges on circularreasoning. Because earlierpapers reporting its presencein passer- the determination of its polarity is not inde- ines. We have also found this muscle to be pendent of other characters,I would hesitate presentin passerinebi•ds, including the Me- to arguepasserine monophyly on this character nuridae and Atrichornithidae (Raikow MS). alone,were that possible. Clearly, the early anatomistsoverlooked this (10) Iliofernoralisexternus absent.--The ab- musclein the passerinesthat they dissected, senceof this hindlimb muscle(under the name probablybecause it is smalland requiresstain- gluteus medius et minimus) was noted by ing to be clearlyvisible. This characteris there- Hudson (1937) on the basis of limited dissec- fore invalid and doesnot supportthe hypoth- tions.It is alsoabsent in variousother groups, esisof passeriformmonophyly. including the Piciformes(Swierczewski 1977, (8) Bicepsslip lacking.--Passeriform birds are Hudson 1937) and Coraciiformes (Maurer and characterizedby 'the absenceof the bicepsslip, Raikow1981). The muscletends to reappearas a muscularbranch that arisesfrom the belly of a developmentalanomaly in passerinebirds the bicepsbrachii and passesthrough the pa- and is even thought to have becomereestab- tagium to join the tendon of the propatagialis lished in some groups(Raikow 1975; Raikow pars Ionga. This structure occurs in many et al. 1979, 1980). The argumentsfor the con- groups of birds. It is also absent in the Corac- cept that the muscle became reestablished in iiformes, however (neither Beddard 1898 nor some passerine groups indicate that its ab~ 438 ROBERTJ. RAIKOW [Auk,Vol. 99 sence is a derived state within Aves. Because oscinesand suboscines.Henley et al. (1978) it is alsoabsent in groupsgenerally considered noted that oscine spermatozoaoccur in bun- close to the passerines, however, one cannot dles and are nonmotileunder certain experi- argue that its apparently primitive absence mental conditions. Feduccia (1979) reported within the Passeriformesis a unique, derived that in two suboscinespecies the spermatozoa condition within Aves; hence, this character are also bundled. The use of this character cannot support the concept of passeriform complex at present is limited because of the monophyly. relatively small number of speciesyet exam- (11) Ambienslacking.--This is the most su- ined and becauseproper outgroup compari- perficial muscle on the medial surface of the sonswill requirethe observationof a diversity thigh. According to Lance Jones (1979), it is of oscine, suboscine,nonpasserine, and non- homologouswith the muscleof the samename avian spermatozoaunder identical laboratory in "reptiles"; therefore, its absencein birds is conditions. The distinctionsare sufficiently a derived state. It is absent in Passeriformes great,however, and the rangeof taxaalready but also in Piciformes,Coraciiformes, Trogon- examined sufficiently broad, that it is a rea- iformes,Apodiformes, and many othergroups sonable conclusion that sperm morphology (George and Berger 1966: 421). Becausethere does corroboratethe hypothesis of passerine is no reasonto supposethat it was lost in Pas- monophyly. seriformesindependently of its lossin any oth- (14) Foot anisodactyl.--Thereare various ar- er group, it cannotbe usedas an argumentfor rangementsof the toes among birds. In the passeriformmonophyly. Passeriformesthe condition is anisodactyl, (12)Iliofemoralis lacking.--Also known as M. meaning that the first toe (hallux) is directed piriformis pars iliofemoralis, this muscle backward, while the second through fourth passesfrom the ilium to the femur. It is present toes are directed forward. This condition oc- in many groups of birds and absent in many cursin the majority of birds, including forms others, including the Passeriformes(George with widely divergentlocomotor habits, while and Berger 1966: 407). Becauseits homology other toe arrangementsare clearly associated with reptilian musclesis uncertain, its polarity with one or another functional specialization. cannot be determined by outgroup compari- For this reason, it appears probable that an- sons. This muscle has been found as an occa- isodactylyis primitive among birds. In addi- sionaldevelopmental anomaly of an apparently tion, this arrangementoccurs in Archaeopteryx atavistic nature in passerine birds, including and in the theropod dinosaurs from which a Fox Sparrow (Passerellailiaca, Raikow 1975) birds are believed by some to have evolved and a White-breasted Wood-swallow (Artamus (Ostrom 1976b). Therefore, this character does leucorhynchus,Raikow et al. 1979). This indi- not constitute an argument for passeriform catesthat the absenceof the musclein passer- monophyly. ines is derived. As there is no reason to believe (15) Phalangealformula 2-3-4-5.--This refers that the muscle was lost in passerines sepa- to the number of phalangesin digits I, II, III, rately from its loss in other birds, however, and IV of the hind limb. The same consider- this characterwill not serveas an argumentfor ations apply here as for anisodactyly;hence, the monophylyof the Passeriformes. this characterdoes not corroboratethe hypoth- (13) Spermatozoabundled, with coiledhead and esis that the order Passeriformesis monophy- largeacrosome.--McFarlane (1963) explored the letic. use of spermatozoanstructure as a taxonomic (16) Hallux incumbent.--This means that the tool, reviewing earlierwork and reportingnew hallux in Passeriformes is at the same level as observations.In nonpasserines,the sperm cells the forward three toes, rather than being ele- are relatively simple in structure, being vated. The polarity of this characteris uncer- straight and having a small acrosome.In con- tain, but, because an incumbent hallux is a trast, the spermatozoaof passerinesare coiled commoncharacteristic among birds, no argu- in the head region and have a large acrosome. ment for its being uniquely derived in passer- The nonpasserinetype is similar to the reptil- ines is possible; hence, it does not corroborate ian condition and hence may be considered passerinemonophyly. primitive within Aves, the passerineform thus (17) Hallux and its claw large.--Among pas- being derived. This condition occursboth in serines,the hallux and its claw are relatively JULY1982] PasseriformMonophyly 439 largein relationto the othertoes, as compared to the condition in most other birds, including •'••EDL FDL the Piciformes and Coraciiformes. The large size of the hallux and its claw may be func- FHL tionally relatedto the degreeof independent actionpermitted the halluxin passerines(ex- cept Eurylaimidae)by the absenceof a con- nection between their major flexors. Ridgway (1901) consideredthe hallux in the Eurylaimi- daeto be relativelyweak, but Olson (1971)dis- counted this. The enlarged hallux appears to be a derived componentof the specializedpas- serineperching foot, which will be discussed in more detail below. Therefore, it apparently does corroborate the idea of passeriform monophyly. ':• FPD2 (18) Type VII deep plantar tendons.--Birds have two deep flexor musclesof the toes, the flexor digitorumlongus (FDL) and flexorhal- lucislongus (FHL) (Fig. 2A). In mostbirds the FDL tendon trifurcates and supplies digits II, III, and IV, so that the muscle flexes these three •"'"" .:__....•• FPD4 digits simultaneously.The hallux is flexed by FHL. There are exceptionsto this, however. In addition, most bird groups have an intercon- nection between the FHL and FDL tendons, Fig. 2. Diagrammaticrepresentation of the ten- either by a tendinous slip (vinculum) passing dons of insertion of the extrinsic digital musclesof from the FHL tendon to the FDL tendon or passerinebirds, the bellies of which, not shown by completefusion of the two tendons.These here, lie in the shank. A. extensordigitorum longus variations in the deep plantar tendons have (EDL); flexordigitorum longus (FDL); and flexorhal- long been used as taxonomiccharacters, es- lucislongus (FHL). A vinculum(v) connectsthe FDL pecially following Garrod (1875) and Gadow and FHL tendons only in the Eurylaimidae (Broad- (1893-1896).Most passerineshave the Type VII bills). B. flexorperforatus digiti II (FPD2);flexor per- arrangementof Gadow's system,with no con- foranset perforatusdigiti II (FPPD2);flexor perforans nection between the FDL and FHL tendons. et perforatusdigiti III (FPPD3);flexor perforatus dig- iti III (FPD3); and flexorperforatus digiti IV (FPD4). Garrod (1875) confirmed earlier observations by Sundevallon this, and later (Garrod1876) included this characteras part of his diagnosis of the Passeriformes. Subsequently, Garrod "reptiles" there is one deep flexor musclethat (1877) reported an exceptionto this condition, supplies all five digits, and the FHL-FDL di- namely the presence of a vinculum in the vision may have arisen in birds or their direct broadbills, Eurylaimidae.He concludedthat reptilian ancestorsalong with the movement either the character must be abandoned or that of the hallux into its opposing position. Also, the Eurylaimidaeare not passerineand chose the character(except for the Eurylaimidae) oc- the first alternative. Subsequentworkers have curs in correlation with other derived states minimized the importance of this character shownby the Passeriformes.Finally, the sep- and have shown that the vinculum is occasion- aration of the two tendons appears to be cor- ally absentin broadbills(see Olson 1971for a related with the enlargedhallux as part of a review). The assumption has been that the functional specializationof the passerinefoot presenceof a vinculum is a primitive stateand (see below). its absence derived. The problem of the Eurylaimidaewould dis- It does appear probable that the lack of a appear if the presenceof the vinculum in that connectionbetween the deep plantar tendons group could be considereda derived (second- is a derived state in birds. At least in some arily primitive) condition.I do not know of any 440 ROBERTJ. RA•icow [Auk, Vol. 99 previous suggestionof this hypothesis,but previous to this study our knowledge of pas- there is good reasonto considerit. The Eury- serine limb muscleswas mostly limited to the laimidae possessa derived stapesmorphology oscines,so that it was difficult to generalize (Feduccia 1975) that clusters them together about the order Passeriformes as a whole. The with most other suboscines as a subclade of speciesof suboscinesdissected, and references the Passeriformes.If the vinculum is primitive, to previousstudies pertinent to the following then the derived stapes of the Eurylaimidae discussion, are listed above under Methods. must have evolved independently of that in M. pubo-ischio-femoralis.--Thislarge muscle other suboscines.Compared to the stapes,the of the thigh passesfrom the postacetabularpel- vinculum is a relatively simple structure.Vari- vis to the femur. In most birds it has two sep- ations in the plantar tendonsof birds are nu- arate bellies, although sometimes these are merousand diverse;members of a singleorder partly or completely fused. In nonpasserines often show considerablediversity. It appears the bellies are arrangedso that one lies more more likely that the vinculum of broadbills or lesscompletely superficially to the other, the evolvedwithin that groupthan that the stapes superficialbelly being calledPars lateralisand is convergent.The feeblevinculum of the Eu- the deep belly Pars medialis. In passerine rylaimidae, in my opinion, is not strong birds, however, one belly lies mostly cranially enough to excludethe Type VII deep plantar to the other, with only slight overlap. Here, tendon arrangementfrom being considereda they are termedPars cranialis and Parscaudalis probable synapomorphyof the Passeriformes. (Baumel et al. 1979). For illustrations of this point compareFigs. IX 52, IX 53, and IX 54 in For each characteranalyzed there are three George and Berger (1966),where this muscle possibleoutcomes: it may corroboratethe hy- is labeled with its old name M. adductor lon- pothesisof passeriformmonophyly, it may fail gus et brevis. It is probable, based on details to corroboratethe hypothesis,or it may refute of their attachments,that the passerinePars the hypothesis.In order to refute the hypoth- esis a character would have to be shown to be cranialisis the homologueof the nonpasserine Pars lateralis, while Pars caudaliscorresponds derived once in a group containingsome pas- to Pars medialis. In any case, the difference serines plus some nonpasserines,but primi- between passerinesand nonpasserinesis dis- tive in other passerines. The alcediniform tinctive. stapeswas originallyargued by Feduccia(1975, The polarity of this differencemust be de- 1977)to be a characterof this type. None of the termined by comparisonswithin Aves, be- 18 traditional charactersanalyzed above was causeI lack information to do outgroup com- found to refute the hypothesis. Five of these parisons with "reptiles." If we accept the characters(numbers 1, 9, 13, 17, and 18) cor- above discussion of the characters as evidence roborate the hypothesis,while the remaining that the order Passeriformesis monophyletic, 13 simply fail to do so. On this basis two then this charactermust alsobe derived by cor- conclusionsmay be made. First, passeriform relation with its common occurrence with monophylyis corroboratedby sometraditional those characters. characterswith sufficient force that it appears In all of the suboscines dissected, this muscle to be a reasonablyviable hypothesis,certainly had the distinctive passerineconditions rather one worthy of further investigation.Second, than the nonpasserineform. This confirmsthe the large numberof traditionalcharacters that descriptiongiven by Hudson (1937)for Corvus fail to supportthe hypothesisunderscores the and Tyrannus. Thus, the form of M. pubo-is- importanceof not assumingthat long recog- chio-femoralisappears to corroboratethe hy- nized taxa are monophyleticin the contem- pothesisof passeriformmonophyly, although poraW sense,merely because they sharesome similarities. I would give it greaterweight if its polarity had been determined by a more independent method than correlation with other characters. THE HIND LIMB MUSCLES Intrinsicfoot muscles.--Birdsin generalhave My preliminary study of some of the hind a set of intrinsic foot muscles that arise from limb musclesof representativesuboscines has the tarsometatarsus and insert on the base of yielded resultsthat contributeto the analysis one or another of the digits. A list of these of passeriformmonophyly. As alreadynoted, musclesand the digits on which they insert is JULY1982] PasseriforrnMonophyly 441
TABLE1. Avian digital muscles.The distributionsshown here are thosefound in the Passeriformesand various other groups.
Intrinsic muscles Extrinsic muscles a
Digit I flexor hallucisbrevis flexor hallucis longus extensorhallucis longus Digit II adductordigiti IIb flexor perforatusdigiti II abductordigiti IIb flexor perforanset perforatusdigiti II [flexordigitorum longus] [extensordigitorum longus] Digit III extensorproprius digiti III b flexor perforatusdigiti III extensorbrevis digiti III • flexor perforanset perforatusdigiti III [flexordigitorum longus] [extensordigitorum longus] Digit IV extensorbrevis digiti IV ½ flexor perforatusdigiti IV adductordigiti IV • [flexordigitorum longus] abductordigiti IV • [extensordigitorum longus] Bracketedmuscles have multiple insertionson different digits in different groupsof birds. Absentin passefinebirds. Absent (occasionallyvestigial) in passefinebirds. given in Table 1, and the function of each is which are widely regardedas being closelyre- given by its name. The number of these mus- lated to the Passeriformes, there are also trends cles varies in different groups of birds, but toward the loss of intrinsic foot muscles. In nonpasserinesgenerally have fairly complete each of these nonpasserineorders, however, sets. George and Berger (1966) and Hudson some families retain at least one of the muscles (1937) record the occurrence of these muscles for each toe, and no families lack the entire set. and give illustrations of them. It was previ- Furthermore, the three orders show the evo- ously known that oscineslack most of these lution of quite different foot adaptations for muscles(summary in Georgeand Berger1966), perching: zygodactylyin Piciformes,anisodac- and our dissections of oscines have confirmed tyly leading to syndactyly in Coraciiformes, this, but little was previously known about and a specializedform of anisodactylyin Pas- suboscines.My dissectionsof the representa- seriformes (discussed below). The greatest tive suboscines listed above confirm the simi- losses of intrinsic foot muscles in the Corac- lar absence of these muscles. iiformes and Piciformes occur in the most de- The intrinsic musclesof the hallux are gen- rived groups (data from Maurer 1977 and erally present in passerines.Except for the oc- Swierczewski 1977). I conclude, therefore, that casional presence of extensorbrevis digiti IV most of the losses of intrinsic foot muscles in in a very reduced (essentiallyvestigial) state, the Passeriformesoccurred independently of however, all of the intrinsic foot muscles of their loss in the other two groups. digits II, III, and IV are lacking in the Passer- ADAPTIVE SIGNIFICANCE OF THE iformes, including both oscines and subos- PASSERINE FOOT cines. This set of muscles as a group is ho- mologousto the intrinsic foot musclesof other In this section I will accept the conclusion tetrapods.Because the classAves is monophy- that the order Passeriformesis monophyletic letic and because these muscles occur both in and will speculatebriefly on the functionaland nonpasserinebirds and in nonavian tetrapods, adaptivesignificance of the passerinefoot. The outgroupcomparison clearly indicates that this hypothesis of monophyly does not depend absenceis a derived state and thereby corrob- upon the validity of these speculations,but orates the hypothesis of passeriform mono- they may help to give some insight into the phyly. biological significanceof certain passeriform It must be noted, however, that the loss of characteristics. all of these musclesmay not have occurredat As a functional mechanism, the passerine one time or at the level of the passeriform foot is distinctively specializedand is probably clade. In the Coraciiformes and Piciformes, a factor in the successof the order in radiating 442 ROBERTJ. RAw,cow [Auk, Vol. 99 into a variety of niches. Basicallythe foot is in the Eurylaimidae,which have a feeblevin- adapted for perchingbut in such a way that culum)presumably allows independent flexion the development of terrestrial habits has not of the forward toes and of the hallux, which been precluded. Perching adaptationshave may aid in the versatility of movementin ad- arisen in a number of ways among birds (see justingthe foot to perchesof varying sizesand Bockand Miller 1959for a generaldiscussion). shapes.This functionalseparation of the flex- The primitive anisodactylfoot has been mod- ion of the forward toes from that of the hallux ified by rearrangingthe digits into zygodactyl is probably associatedwith the enlarged size or heterodactylconfigurations, or by joining of the hallux as part of the passerineperching some of the forward toes at their basesin syn- specialization.These extrinsic musclesEDL, dactyly.In differentways thesemodifications FDL, and FIlL are always present. enhancethe use of the foot as a graspingmech- Each forward toe also has one or two indi- anism.Among passerines,one modificationof vidual extrinsic flexor muscles that insert at the retained primitive anisodactylfoot is the one or more pointsalong the plantarsurface of enlargementof the hallux, which presumably the digit, flexing it around one or anotherin- provides a more evenly balanceddistribution terphalangealjoint. These muscles,together of strengthbetween the numericallyunequal with the FDL, permit varying patternsof flex- opposingsets of toesand permitsthe halluxto ion, so that the toes can conform to perchesof encirclethe perch effectivelyin opposition to different sizes and shapes.These musclesare the other toes. the flexorperforatus digiti II (FPD2),flexor per- The most striking aspectof the evolutionof forans et perforatusdigiti II (FPPD2), flexor the passerinefoot is the loss of the intrinsic perforatusdigiti III (FPD3),flexor perforans et muscles of the forward toes as described perforatusdigiti III (FPPD3),and flexorperfor- above. The pattern of lossesand their func- atus digiti IV (FPD4) (seeTable 1 and Fig. 2B). tional consequencesmay be understood by Again, these musclesare always present in consideringthe generalstructure of the limb. passerinebirds. Extrinsic muscles.--There are a number of Thus, the extrinsicflexor systemconsists of muscles activating the toes, the bellies of one musclethat providessimultaneous flexion which lie in the shankand that may therefore of the forward three toes, plus individual flex- be termed extrinsic foot muscles. The three for- ors of each forward toe, and an independent ward toes have a common extensor, M. exten- flexor of the hallux. The extrinsic extensorsys- sor digitorum longus (EDL), the tendon of tem is simpler, as there are no individual ex- which passesacross the intertarsal joint and tensors,only the commonextensor of the for- down the dorsal surface of the tarsometatarsus ward three toes. This entire extrinsic muscle (Fig. 2A). Near the distal end of that bone, the systemis always present in passerines,appar- tendon trifurcates, the branchesinserting on ently representinga necessaryminimum of the dorsal surfaces of the three forward toes. complexity. Thus, the EDL provides for simultaneousex- Intrinsic muscles.--As discussed earlier, non- tensionof thesedigits. There is alsoa common passerinebirds have intrinsicfoot musclesthat flexor, M. flexor digitorum longus (FDL), the arise on the tarsometatarsus and insert at the tendon of which passesdown the plantar sur- bases of the forward three toes, while in pas- face of the tarsometatarsus,trifurcating dis- serinesthis entire set is lost exceptfor one oc- tally to insert on the plantar surfacesof the casionalvestige. The order Passeriformesis three forward toes (Fig. 2A). This provides si- thereforecharacterized by a major simplifica- multaneousflexion of thesedigits. Thus, these tion of the foot mechanism. two muscles produce simultaneousextension The hallux opposesthe forward toes and, as and flexion of the forward three toes. The hal- noted above,has a singleextrinsic flexor, FIlL. lux is likewise providedwith an extrinsicflexor It also has two intrinsic muscles(Fig. 3). The muscle, the flexor hallucis longus (FHL), but intrinsic extensor,M. extensorhallucis longus it has no extrinsicextensor in birds (Fig. 2A). (EHL), is the only extensorof the hallux, as In most passerinebirds the tendonsof the FIlL there is no extrinsic extensor in birds, and it and FDL have no interconnectionas they pass is never lost. The intrinsic flexor, M. flexor hal- down the plantarsurface of the tarsus,as noted lucisbrevis (FHB), is a synergistof the much above. The absenceof this connection(except largerFHL. JvL¾1982] PasseriformMonophyly 443
The forward toes have the capacity for si- multaneous extension and for simultaneous or individual flexion, including variation in shapingthe flexeddigits to fit the perch.The loss of the intrinsic forward toe muscles, how- ever, eliminates a repertoire of individual ab- duction, adduction, and extension move- ments. Passerines have thus retained a variable mechanismfor graspingbut have simplified the rangeof movementsnot associateddirectly with the grip. This presumablylimits the func- tional capabilitiesof the foot where suchsubtle movementsmight be useful, such as in walk- ing or climbing over irregular surfacesor graspingvariously and irregularly shapedob- jects. The passerinecondition is in striking contrast,for example,to the complexityof the Fig. 3. Diagrammaticrepresentation of the two intrinsic foot musculature of mousebirds (Co- intrinsic foot musclesgenerally found in passerine liiformes), which hold food with their feet and birds, M. extensorhallucis longus (EHL) and M. flex- have an astonishingvariety of movementsand or hallucis brevis (FHB). postures(Berman and Raikow 1981). Clearly, passerinesdo not depend upon these capabil- ities; the bill is the usual manipulative organ, largerFHL. On theother hand, passerines with and passerinesare prone to fly even short dis- tances rather than clamber over difficult ter- a stronggrip may have considerableenlarge- ment of the intrinsic hallux musclesalong with rain. other modifications, such as were discussed The loss or major reduction of foot muscles previouslyin the shrikes(Laniidae) (Raikow in passerine birds tends to occur in certain pat- et al. 1980). terns not unlike those describedby Stegmann
(1978) in the avian forelimb: muscles that are CONCLUSIONS reduced or lost tend to be those that (1) are initially small in size; (2) are complementary Some readers of an earlier version of this to others in their actions, so that their loss may paper suggestedthat this analysisis hardly reduce the subtlety or variety of some move- necessary,because the order Passeriformesis ments but will not eliminate an action entirely; almostuniversally recognizedas being mono- and (3) are usuallysmaller in size and simpler phyletic. One found my argumentsquite un- in structure(e.g. crossingfewer joints) than convincingbut agreedwith my conclusions. their synergiststhat are retained. To this I have two responses.First, the concept Adaptive potential.--Nevertheless,although of monophyly often employed is vague and passerineshave a limb muscle systemgreatly imprecise.Second, previous studies have am- simplified in many respects,it does retain the ply demonstratedthat many traditionallyrec- capabilityof someadaptive variation. There is ognizedtaxa are not monophyleticin the strict much variety in the two intrinsic musclesof and meaningfulsense, and thereforeI urgethat the hallux. The EHL is never lost, presumably suchassumptions should not be made. I men- becauseit has no synergistand its losswould tion thesepoints becausethey illustrate a com- eliminate the necessaryability to extend the mon tendencyfor biologiststo assumethat tra- hallux. In the Ocellated Tapaculo (Acropternis ditionaltaxa are monophyletic,perhaps because orthonyx:Rhinocryptidae), however, it is re- that which is familiar tendsto appear"natural" duced to a vestige, probably in association in some sense. with the terrestrial habits of this species.The The task of systematicbiology is to produce intrinsic flexor, FHB, is lost entirely in this hypotheses of phylogenetic relationships speciesand is often reduced to a vestige in amongorganisms, and the key to doingthis is passerines.Presumably this muscleis dispens- the ability to recognizemonophyletic groups. able, becauseit is a smallsynergist of the much The chief virtue of the dadistic school in con- 444 ROBERTJ. RAIKOW [Auk,Vol. 99 trast to others is not that it accomplishesthis BORECKY,S. R. 1977ßThe appendicularmyology and goal more satisfactorily,although it does, but phylogenetic relationshipsof the avian "corvid that its methodologypermits the full exposure assemblage." Unpublished Ph.D. dissertation. of every facetof an analysisfor maximumease Pittsburgh,Pennsylvania, Univ. Pittsburgh. --. 1978. Evidence for the removal of Pseudo- of criticism.As a result,a hypothesis,like the podoceshumills from the Corvidae. Bull. Brit. one of passerinemonophyly discussed herein, Ornithol. Club. 98: 36-37. may be seen to rest on individual arguments ELDREDGE,N., & J. CRACRAFT.1980. Phylogenetic that vary in their strength,weakness, and de- patterns and the evolutionary process. New gree of ambiguity. York, Columbia Univ. Press. On the basis of the argumentspresented in FEDUCCIA,A. 1975. Morphology of the bony stapes this paper I concludethat the order Passeri- (columella) in the Passeriformes and related formes,originally defined as a pheneticcluster, groups:evolutionary implications. Univ. Kansas is a cladeor monophyleticgroup in the specific Mus. Nat. Hist., Misc. Publ. No. 63. contemporary sense. --. 1977. A modelfor the evolution of perching birds. Syst. Zool. 26: 19-31. --. 1979. Commentson the phylogenyof perch- ACKNOWLEDGMENTS ing birds. Proc. Biol. Soc. Washington92: 689- 696. For the loanof specimensI wish to thankMary H. Clenchand KennethC. Parkes(Carnegie Museum GAFFNEY,E. S. 1979. An introduction to the logic of Natural History)and CharlesG. Sibley(Peabody of phylogenyreconstruction. Pp. 79-111 in Phy- Museumof Natural History, Yale University).Mary logenetic analysis and paleontology.J. Cracraft H. Clench, Joel Cracraft, StorrsL. Olson, Kenneth C. and N. Eldredge, Eds. New York, Columbia Univ. Press. Parkes,and an anonymousreviewer provided ex- tremely helpful criticismsof the manuscript. This GADOW,H. 1893-1896. Muscular system. Pp. 602- doesnot mean that they all agreewith everything 620 in A dictionary of birds (A. Newton, Ed.). written here or, for that matter, with each other. This London, Adam and Charles Black. work was supportedby National ScienceFoundation GARROD,A. H. 1875. On the disposition of the deep grants DEB-7810715and DEB-8010898. plantar tendons in different birds. Proc. Zool. Soc. London: 339-348. --. 1876. On some anatomical characters which LITERATURE CITED bear upon the major divisions of the passerine BAUMEL,J. J., A. S. KING, A.M. LUCAS,J. E. BREA- birds. Part I. Proc. Zool. Soc. London: 506-519. ZILE, & H. E. EVANS (Eds.). 1979. Nomina An- ß 1877. Notes on the anatomy of passefine atomica Avium. London, Academic Pressß birds. Part II. Proc. Zool. Soc. London: 447-452. BEDDARD,F. E. 1898. The structure and classification GEORGE,J. C., & g. J. BERGERß1966. Avian myology. of birds. London, Longmans,Green, and Com- New York and London, Academic Press. panyß GLENNY,F. H. 1955. Modifications of pattern in the BENTZ,G. D. 1976. The appendicularmyology and aortic arch systemof birds and their phyloge- phylogeneticrelationships of the Ploceidaeand netic significance. U.S. Natl. Mus. Proc. 104: Estrildidae (Aves: Passefiformes).Unpublished 525-621. PhßD. dissertation. Pittsburgh, Pennsylvania, HENLEY, C., A. FEDUCCIA,• D. P. COSTELLOß1978ß Univß Pittsburghß Oscine spermatozoa:a light- and electron-mi- --. 1979ßThe appendicularmyology and phy- croscopystudy. Condor 80: 41-48. logeneticrelationships of the Ploceidaeand Es- HUDSON, G. E. 1937. Studies on the muscles of the tfildidae (Aves: Passeriformes).Bull. Carnegie pelvic appendagein birds. Amer. Midi. Natur. Mus. Nat. Hist. No. 15. 18: 1-108. BERGER,g. J. 1956ßThe expansor secundariorum HUXLEY, T. H. 1867. On the classification of birds; muscle, with special reference to passerine and on the taxonomic value of the modifications birds. J. Morphol. 99: 137-168. of certain of the cranial bones observable in that BEllMAN,S. L., & R. J. RAIKOW.1982. The hind limb class. Proc. Zool. Soc. London 1867: 415-472. musculature of the Coliiformes. Auk 99: 41-57. LANCEJONES, C. 1979. The morphogenesisof the BOCK,W. J., & A. MCEvE¾.1969ß Osteology of Ped- thigh of the mousewith specialreference to tet- ionomustorquatus (Aves: Pedionomidae)and its rapod musclehomologies. J. Morphol. 162: 275- alliesßProc. Royal Soc. Victoria 82: 187-232. 310. --, & W. D. MILLER. 1959ß The scansoffal foot MAURER,D. R. 1977. The appendicularmyology and of the woodpeckers,with commentson the evo- relationships of the avian order Coraciiformes. lution of perching and climbing feet in birds. Unpublished Ph.D. dissertation. Pittsburgh, Amer. Mus. Novitates, No. 1931. Pennsylvania,Univ. Pittsburgh. JVL¾1982] PasseriformMonophyly 445
--, & R. J. R•I