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Phylogenetic Analysis of the Nest Architecture of Neotropical Ovenbirds (Furnariidae)

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The Auk 116(4):891-911, 1999 PHYLOGENETIC ANALYSIS OF THE NEST ARCHITECTURE OF NEOTROPICAL OVENBIRDS (FURNARIIDAE) KRZYSZTOF ZYSKOWSKI • AND RICHARD O. PRUM NaturalHistory Museum and Department of Ecologyand Evolutionary Biology, University of Kansas,Lawrence, Kansas66045, USA ABSTRACT.--Wereviewed the tremendousarchitectural diversity of ovenbird(Furnari- idae) nestsbased on literature,museum collections, and new field observations.With few exceptions,furnariids exhibited low intraspecificvariation for the nestcharacters hypothe- sized,with the majorityof variationbeing hierarchicallydistributed among taxa. We hy- pothesizednest homologies for 168species in 41 genera(ca. 70% of all speciesand genera) and codedthem as 24 derivedcharacters. Forty-eight most-parsimonious trees (41 steps,CI = 0.98, RC = 0.97) resultedfrom a parsimonyanalysis of the equallyweighted characters using PAUP,with the Dendrocolaptidaeand Formicarioideaas successiveoutgroups. The strict-consensustopology based on thesetrees contained 15 cladesrepresenting both tra- ditionaltaxa and novelphylogenetic groupings. Comparisons with the outgroupsdemon- stratethat cavitynesting is plesiomorphicto the furnariids.In the two lineageswhere the primitivecavity nest has been lost, novel nest structures have evolved to enclosethe nest contents:the clayoven of Furnariusand the domedvegetative nest of the synallaxineclade. Althoughour phylogenetichypothesis should be consideredas a heuristicprediction to be testedsubsequently by additionalcharacter evidence, this first cladisticanalysis of the fur- nariids demonstratesthe generalutility of nest charactersin reconstructionof avian rela- tionships,and it providesa testof monophylyfor several furnariid taxa. Received 29July 1998, accepted12 March 1999. RECENT APPLICATIONS OF PHYLOGENETIC SYS- a broad diversityand complexityof neststruc- TEMATICSto ethologyhave demonstratedthat tures. behavioraltraits can be as historicallyinfor- The suboscinefamily Furnariidae,with 240 mativeas morphologicaland molecularchar- currently recognized biological species, is acters(Prum 1990, de Queiroz and Wimberger amongthe mostmorphologically, behaviorally, 1993,Paterson et al. 1995,Irwin 1996,Kennedy and ecologicallydiverse families of passerines et al. 1996).Nests are a detailedpart of the ex- (Ridgelyand Tudor 1994, Skutch1996). The tendedphenotype of birds,and they providea furnariid radiationincludes phenotypes con- durablephysical record of the behaviorthat re- vergenton numerousfamilies of oscines,such sultedin their construction(Hansell 1984, Col- aslarks, jays, tits, creepers,nuthatches, wrens, lias 1986).A wealth of quantifiabledetail in thrushes, thrashers, dippers, and warblers neststructure, placement, and ontogenymakes (Leisler1977). Representatives of the Furnari- nests amenableto comparativeanalysis. Nest idae can be foundin all Neotropicalhabitats, architecturecan provide evidence of phyloge- fromcoastal surf zone and sand dunes through netic relationships(Kiff 1977, Lanyon 1986, dry andhumid lowlandand montane forests to Prum 1993,Whitney et al. 1996).Furthermore, the treelesspuna of the Andes. hypothesesof phylogenycan be used to dis- The diversityof nestplacement and structure coverhistorical patterns in the evolutionof nest in the Furnariidaeapproaches that of theentire featuresand to test hypothesesabout adapta- order Passeriformes(Narosky et al. 1983,Sick tion in nest design (Dekker and Brom 1992, 1993,Collias 1997).Nests can be placedin ex- Winklet and Sheldon 1993, Lee et al. 1996, cavatedor adoptedcavities under or abovethe Eberhard1998, Sturmbauer et al. 1998).Here, ground. Non-cavity nests can be supported we use nest architectureto generatea hypoth- from below,attached by the side to a vertical esisof phylogeneticrelationships for the Neo- support,or suspendedfrom a branchor rock. tropicalovenbirds (Furnariidae), which exhibit Nest structuraldiversity ranges from shallow pads of looselypiled material to domednests E-mail: [email protected] with constructed roofs of interlaced sticks, in- 891 892 Z¾SKOWSK•AND PRUM [Auk, Vol. 116 terwoven soft vegetation, or clay. Additional nariidae + Dendrocolaptidaeis a clade com- elaborations of domed nests include entrance posedof the Formicariidae,Conopophagidae, tubes, tunnels with constrictions,awnings and Rhinocryptidae(i.e. Formicarioideasensu above the entrance,nonbreeding chambers, Sibleyand Ahlquist1990). and adornmentwith conspicuousobjects. The genericlimits within Furnariidaerec- Over the last century,architectural features ognizedin this study follow thoseof Peters of furnariidnests have been recognized to be (1951), with a few modificationsfollowing evolutionarilyconservative, constituting poten- Ridgely and Tudor (1994) and Kratter and tially informativesystematic characters (Iher- Parker(1997). Since the publicationof Peters' ing 1914, 1915; Vaurie 1971, 1980). However, (1951)volume, a surprising14 new speciesand previousauthors have used nest architecture in 1 new genusof furnariidshave been described, an eclectic,noncladistic manner; no compre- 14 subspecieshave been elevated to therank of hensivephylogenetic analysis of thefurnariids species,and 5 specieshave been synonymized hasbeen conducted, preventing rigorous study (Ridgelyand Tudor 1994,Pacheco and Gonza- of the evolution of nest-construction behavior. ga 1995,Silva 1995,Pacheco et al. 1996,Maijer Detailedhypotheses of hornologyamong nest and Fjelds• 1997, Zimmer 1997).As currently typeshave proven difficult to developbecause recognized,the Furnariidae consists of 240spe- of limited information about many species, ciesin 59 genera. paucityof behavioralinformation on the steps of nestbuilding (i.e. ontogeny),and the histor- METHODS ical lackof a phylogeneticmethodology. Data.--Variation in nest architecture of furnariids Our objectivewas to examinepatterns of var- iation in nest structure and construction behav- and outgrouptaxa was reviewedbased on the sci- entific literature and on data associated with nest ior within theFurnariidae and to performa cla- and egg specimensin majorcollections. The first au- disticanalysis of the family basedon nestchar- thor examinednest specimens in majorNew World acters.We performedthis analysisto yield hy- collections(see Appendix 1) and collectednew data pothesesof phylogeneticrelationships of major describing204 nestsfrom 53 speciesduring his field cladeswithin the family and to evaluatethe studiesin Peru,Brazil, Paraguay,and Guyana(1994 usefulnessof nestcharacters for reconstructing to 1998).Results of the field work, includingnew on- avian phylogenies.We also proposeand dis- togeneticinformation and nest descriptionsfor sev- cussnew hypothesesregarding the evolution en specieswith previouslyundescribed nests, will be of furnariid nest-construction behavior publishedseparately. Nest informationwas gatheredfor 184 furnariid Reviewof furnariid systematics.--The Furnari- speciesfrom 50 genera;species for which nest de- idaeis a family of tracheophonesuboscine pas- scriptionswere demonstrablyerroneous or lacking serinesclosely related to the woodcreepers criticaldetails were subsequentlyexcluded. Data for (Dendrocolaptidae).The two familiesshare a the remaining168 species,representing 41 genera unique intrinsic syringeal muscle, M. vocalis (ca.70% of all speciesand genera),were used in the dorsalis(Ames 1971). Monophyly of the Den- analysis(Appendix 2). A completelist of sourcesof drocolaptidaehas been supported by morpho- nestdescriptions for eachspecies is presentedin Ap- logicalsynapomorphies (Raikow 1994, Clench pendix1. Samplesizes varied considerably, with ap- proximately5% of the speciesrepresented by more 1995), but no morphologicalsynapomorphy than 50 nestseach, the majorityof speciesbased on satisfactorilydemonstrates the monophylyof more than 10 nests,and about 20% of the species the furnariids.Morphological characters tradi- known from a singlenest description. tionally used to diagnosethe family (e.g.lack We also assemblednest informationfor outgroup of hornson the processivocales [Ames 1971] taxa: 37 speciesrepresenting all 13 generaof Den- andpseudoschizorhinal nares [Feduccia 1973]) drocolaptidae;19 speciesrepresenting 8 of 12 genera are primitive amongtracheophones, and none of Rhinocryptidae;19 speciesrepresenting all 7 gen- is shared by all furnariid species(Feduccia era of Formicariidae;and 5 of the 8 speciesof Cono- pophagidae. 1973).We assumedthat the Furnariidaeand the Phylogeneticanalysis.--The number of ingrouptaxa Dendrocolaptidaeare eachmonophyletic and was reduced to 49 operational taxonomic units are sistertaxa, basedon the Sibley and Ahl- (OTU) by combiningcongeneric species having iden- quist(1990) DNA-DNA hybridizationhypoth- tical characterstates. Appendix 2 includesdefini- esis.The hypothesized sister group to theFur- tions of speciesgroups composedof behaviorally October1999] NestPhylogeny ofFurnariidae 893 similarcongeners used as OTUs. The outgroupspe- data that are consistent with those of their bet- cies were condensedinto two OTUs representing ter knowncongeners are presumed to be mem- two successiveoutgroups, Dendrocolaptidae and bersof the sameOTU (seeAppendix 2). Formicarioidea. Webased hypotheses of behavioralhomologies on 1. Nest in cavity.--Thenest is placed in an specialdetailed similarities in neststructure and on- adoptedor self-excavatedcavity, such as a sub- togenyof nestconstruction. Variations in nestarchi- terranean burrow, rock crevice, termite mound, tecture were coded as 24 characters, of which 22 were tree
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    UNIVERSIDAD NACIONAL MAYOR DE SAN MARCOS FACULTAD DE MEDICINA VETERINARIA UNIDAD DE POST GRADO Vigilancia dirigida de influenza aviar en aves silvestres de los humedales de Puerto Viejo usando patos domésticos (Cairina moschata) como centinelas TESIS para optar el grado de magíster en Salud Animal AUTOR Juan Alexander Rondón Espinoza Lima-Perú 2011 Dedicado a: Mis padres Tula y Manuel, viejitos desde aquí les mando esta dedicatoria con todo mi amor para ustedes que están en el cielo. Mis hermanos Manuel y Alfredo, les agradezco por haber compartido el tiempo de mi niñez con ustedes, un abrazo imaginario para los dos. Mis hermanos Erwin, Tula, Ricardo e Ysabel, a ustedes que comparten conmigo su cariño, sus alegrías y tristezas…, los quiero mucho. Mis sobrinos Miguelito, Yair y Franco, a ustedes que con sus travesuras me hicieron volver a mi niñez, haciéndome reír. ¡Gracias a ustedes por ser mi familia! Este trabajo también está dedicado a ti joven estudiante; - Que, desde muy niño tuviste muchos obstáculos y problemas por muchos motivos y, cuando creciste tuviste carencias de comodidades, pero a la vez fuiste consciente de eso y supiste afrontarlo de alguna manera, no dejando de luchar por alcanzar tus metas. - Que, supiste encontrar solo tu camino con ayuda de tus seres queridos, y que a pesar de quererlos mucho, no fuiste un hijito de papá, ni de mamá. - Que, para avanzar supiste agradecer y retribuir todo lo que te dieron alguna vez las personas cercanas (familia, amigos, conocidos, etc.). - Que, para trabajar en grupo, siempre ofreciste y ofreces buena voluntad, dedicación, y sobretodo cumpliste con la ley del amor impersonal, dando lo mejor de ti en todo lo que haces.