Effects of a cold wave on an Amazonian avifauna in the upper Paraguay drainage, Western Mato Grosso, and suggestions on Oscine-Suboscine relationships Edwin O'Neill Willis (*) Abstract de Bugres. East of Barra de BugrE.s, the remarmng vegetation is mostly dry forest The avüauna of the forested upper reaches of grading into cerrado and pantanal. From Barra the Sopotuba River. in the upper Paraguay drainage just south of the Serra dos Parecís, proved a de Bugres westward. the foresr is rapidly rnixture of central-Amazonian birds from just east being cut. of the Madeira Rtver and of birds of dry forests Since birds of the Paraguay-drained eastern (Xingú-Tapajóz) or lower Andean forests peripheral part of this forest had only been studied to the southern Amazonian region. A cold wave that passed during the study period caused a major briefly by Natterer (in Pelzeln, 1867) and by drop in insect activity and in the activity of inseci Naumburg (1930) and coworkers, I welcomed -eating birds and hummingbirds. Fruit-eating birds an opportunity to look at birds there on an and "omnivores" (insect and fruit eaters) became expedition of the Zoology Department of the relatively conspicuC'Ius. It is suggested that occasio· Universidade Estadual de Campinas (UNICAMP) nal "clisasters" of the type of a cold wave inhibit specialized insectivores at this and other margins from 11 to 21 July, 1975. During our vísit, a of Amazonian forests, and encourage hJgher percen major cold wave or friagem swept north, tages of omnivores. The previously noted tendency bringing frost and snow to souther~ Brazil and for oscines to replace suboscines at various types ending as floods in northeastern Br&,·il. This of neotropical forest rnargins ls reinterpreted as offered an opportunity to look at the effects prlmarily due to declines of furnarioid suboscines (mostly forest-livmg insectivores> and their repla of a friagem at the southern margin of the cement by omnivf)rous tyrannoid suboscines anel Amazonian forest, and contrast observations by omnivorous oscines. The conventional theory with previously reported minar effects of cold that furnarioid suboscines are prirnitive and that waves well to the north (such as Bates, 1962: they and other neotropical suboscines are being 330). pushed into forests by recently immigrating oscines leads to two ecological anomalies: virtual absence Here I gfve the species observed, and by of omnlvorous passerines in the carly Cenozoic an:i means of daily counts of individuais and absence of seed-eat.ing passerines for much of the species eating various foods illustrate certain late Cenozoic. As alternate theory, that of separa effects of the cold wave which, magnified in tion of forest-edge suboscines by continental dritr followed by evolut.ion of forest-dwelling furnarioid reglons of greater altitude or farther south, suboscines in the New World, with open-country could lead to such oft-reported avifaunal oscines either separated by the drift or entering phenomena as replacement of suboscine by South America early in the Ceno.zoic, removes both oscine Passeriformes at various kinds of anomalies. borders of neotropical forests (Siud, 1960; Novaes, 1973). In western Mato Grosso, a narrow penín sula of Amazoni:an forest follows the Guaporé LOCALES AND CHRONOLOGY River southward and eastward on the south side of the Serra dos Parecís, a c2mpo or Few patches of forest remain along the cerrado-covered plateau of some 500 me road from Barra de Bugres 70 km west to the ters'elevation. This forest península once plateau town of Tangará da Serra. July 11 re.ached east into the drainage of the upper and 12, the UNICAMP expedition visited forest Paraguay River, at least to the town of Barra remnants at about 150 m elevation and 30 km ( • ) - Universidade Estadual de Campinas, SP. ACTA AMAZONICA fl(3) : 379-394 - 379 W of Barra de Bugres. plus continuous zones in waves of dark and light gray, and instead of seasonally flooded woodlands (várzea) of rain there was a steady rush of wind along the small Branco Rivcr just south. July twisting the treetops. Temperaturas dropped 13 and 14, after crossi ng a zone of dry very slowly, even with the constant wind and wood!ands and of cerrado on a spur ("Serra with the undulating canopy of cloud$ racing dos Cinquenta ") of the Serra at and east of northward. The trees near ou r camp Qroaned Tangará, we visited large patches of recently and there was a !ight drizzle much of the night, logged forest on the east side of the Sopotuba but the morning of the 17th was only moder Ri ver (spelled "Sepotuba" and oi'her variants ately cool. At dawn, birds were normally noisy. by Pelzeln, 1867, and Naumburg, 1930) some However, the wi!"ld and clo:.Jds continued to 20 km W of Tangará. hurry north, and temperatures barely rose July 15 to 17 we worked in sandier but beyond the low night levei. Not one of the extensive low woodlands some 30 to 40 km stingless bees and "African" bees, a constant NW of Tangará and beyond the Sopotuba River, nuisance in the sandy forest the preceding on the road from the Maracanã River to the two days, appeared the whole day. Two "Fazenda do Português". Near the sandstone colonies of army ants (Eciton burchelli) under cliffs of the Serra, some areas are very sandy, observation failed to move the whole day, and for instance, one area of Jow scrub and individuais responded as if in slow moticn scrub-woodland supported singing Rhytipterna even when di5turbed. Even when the sun immunda, a bird that near Manaus occurs in appeared about 13:00 hardly a butterfly moved structurally similar sandy "campinas" (Lisbôa, along the road. 1975) and in Surinam in sand-ridge scrubland Clear skies continued after the front (Haverschmidt, 1975). passed. By 16:00 temperaturas were dropping July 18 we investigated forest remnants rapidly. Night temperaturas apparently reachf'd 20 km SW of Tangará, near Fazenda Tapirapoã below 3° C (temperatura recorded in Cuiabá, on the Sopotuba River. July 19-20 we visited at 150 m elevation), with light frost reported tall forests being cleared on Fazenda Arapi from the tips of leaves of coffee sprouts. The tanga, about 30 km NE of town on the Sopotu following morning was very cold, anti forest binho River. Most of the forests on these birds silent. Grndually temperatures rose. but days, as on July 13-14, were on deep clay the day was still cold and insect-free. riverin soils and at 200-350 m elevation. July July 19 and 20 day temperaturas in the 21 we returned to the wooded patches 30 km forest continued decidedly cool, much like W of Barra de Bugres. those of a subtropical forest. A colony of army ants started swarming only just before noon 'I'HE "FRIAGEM" on July 19, and the ants moved 6 m per hour rather than the usual 15 or so. July 20 the July is the middle of the long dry winter ants started about 09:30, and traveled about in western Mato Grosso, Skies are normally 1O m per hour. Butterfly and other insect cloudless, night temperaturas cool, and day activity seemed fairly high after noon on July temperaturas high. July 11-16 temperaturas 19 and after about midmorning on July 20, but became steadily warmer, reaching about 35° C on the second day many butterflies were dying at midday. At 15:00 on July 16, undulating on the road. dark clouds suddenly covered the southern sky and approached rapidly. At 16:00 wave THE AVIFAUNA, .'\ND EFFECTS OF THE COLO WAVE after wave of Whiteeyed Parakeets (Aratinga leucophthalma) carne high 011er, headed In the Appendix, species of birds observed northward with constant gabble. I estimated are listed as well as numbers of individuais that some 500 birds crossed within my sight seen or heard in the indicated numbers of from a narrow road through low forest. The hours afield each day. A birêl marked (?) is clouds were Jess black as they carne overhead probably the spccies indicated, but could be 380- WUHs close relative of it. The list follows Meyer de Table 2 separates the birds by food types Schauensee (1970) even when !ater revisers A through D. Some of the insectivores" may u or my own observations suggest a different also eat some fruits, as diets of most species taxonomy. Types of food are indicated for are not well known. each family as follows: A, nectar and insect Hummingbirds (Type A) most strongly feeders: B, fruit or seed eaters; C, fruit and showed effects of the cold wave. None was insect eaters; D. insectivores; E, carnivores seen on the 17th, one on the 18th, and one other than insectivores. When a species differs (a Heliomaster furcifer very weak of flight in from the majority of its family, the fcod type a sunlit treetop) on the 19th. Fair numbers is indicated after its name. Food types are were active at well-lighted treetop sites and from Haverschmidt (1968) and other authors, in some areas of undergrowth on the 20th. plus my own observations. Hummingbirds are known to enter torpor at Table 1 totais counts of species and night and during cold periods, and it is possible individuais of food types A through D for the that some individuais did so during much of days July 13-20, when we were working in the cold wave. fairly comparable areas close to Tangará da Fruit-eating birds remained active and Serra. More detailed analyses, such as timed fairly conspicuous decreasing in absolute census runs in the same area, were not numbers seen but rising slightly in percentage possible both because I did not know that a of the avifauna, from the normal 10 or 15 cold wave would pass and because we had to percent of species to about 20 percent on the move about for the research of others in the 18th, and from the normal 25 percent of the group. individuais seen to 40 percent on that day and Table 1 indicates that on the two coldest the next. days, July 17 and 18, the number of specie& "Omnivorous" birds, eating fruit and observed was about one-half of normal and insects, were less frequently observec! during the number of individuais about one-third of the cold wave but remained at about the usual normal. (The waves of parakeets rai&ed the percentages of the avifauna - 40 percent of total unduly on July 16; probably 50 or less of the species and slightly over 35 percent of the 500 would have been seen on an crdinary the individuais. These species continued day, and 50 i s the number used here for certa in active and fairly conspicuous, but flocked to comparisons). Specifically, after the normal!y fruiting trees instead of hunting insects (except noisy dawn of July 17 (indicating that cold in sunlit areas at the warmest hours of after itself did not dampen calling and song until the noon. when they stayed close to the fruit trees birds had to look for food). forest birds became in their hunts). silent and hard to locate. Parrots and pigeons lnsectivorous birds were quiet and incon continued relatively noisy, but even th::>y were spicuous, though the few seen seemed to rather silent July 18. On July 19 and 20, the forage actively. Percentages decreased from amount of calling increased to leveis possibly a normal species percentage of 40 to 31 on but not clearly below the usual forest levei. the 18th, and from a normal 35 or so percent TA.BLE 1 Species and Individuais of Forest Birds July 11 12 13 14 15 16 17 18 19 20 21 ~pecies 61 103 91 106 114 92 50 42 94 119 87 Indivttluals 191 560 409 552 526 859• 157 161 490 746 461 o. 409 i f ~ome 450 "extro" porokccts ore excluded (see tc><t). Effects of a cold wnve - 381 of individuais to 22 percent on that day. Birds O. picumnus to north, south, northeast, and that follow army ants disappeared completely west. (Local distribution 'lf birds of this group July 17-18, and did not even apear near inactive is complex. For instance, Naumburg, 1930, bivouacs during my visits. Mixed-~pecies reports that near Tangará the related D. flocks were smaller than usual, and severa! platyrostris wedges in from the east, pre were at sunny areas overgrown with vinss at sumably in gallery woodlands on the open edges of the forest. Torpor or major mortality planalto of the Serra, and O. picumnus seems unlikely; probably the birds were simply pal/escens wedges up from the south, in pan less conspicuous. tanal or semiopen woodlands). Hyle><etastes perroti uniformis is widespread between the Madeira and the Xingú, but is replaced by H. A.FFINITIES OF THE TANGA..~ DE SERRA FAUNA stresemanni westward. The Dendrocincla The analyzable avifauna (species other fuliginosa observed here were probably of the than widely distributed ones without dis· subspecies atrothorax from between the Ma tinctive subspecies) of the forests near Tan deira and Tapajóz Rivers, for they were gará da Serra is most closely related to the streaked and had the unusual call character avifauna of forests east of the rio Madeira, istic of this subspecies; this subspccies is but shows some elements from other regions, already known from the Guaporé River (I do such as lower Andean forests and dry forests not, however. know O. f. trumaii from the south and east of the Tapajóz River. The re upper Tapajóz-Xingú region, and suspect it lationships are most clearly shown by birds may not be distinguishable in the field). The that regularly follow army ants, fcr most occur Oendrocincla merula seemed of the subspecies only or mainly east of the Madeira: o/ivascens from the Madeira to the Tapajóz, Rhegmatorhina hoffmannsi, an anl-follow· not of bartletti or remota from west of the ing species of the east bank of the Madeira, Madeira nor of castanoptera from east of the is replaced by related species west of the Tapajóz. Ph/egopsis nigromaculata seemed Madeira and on both sides of the lower Tapa of the large-spotted and white-sided form józ (Willis, 1969). Oendroco/aptes hoffmannsi bowmani, which ranges from the Madeira to ranges from the Madeira to the Xingú. and is the Xingú. The-;e species or distinctive sub replaced by different subspecies of the related species suggest entrance of the avifauna east TABLE 2 Percentages of Species and Individuais of Forest Birds by Food Type July 13 14 15 16 17 18 19 20 SPECIES% Hummingbirds 2 5 8 4 o 2 1 3 Frugivores 16 14 12 10 14 21 14 11 Fruit/Insects 40 39 39 42 40 43 38 41 Insectivores 39 42 39 39 40 31 45 43 Others 3 o 3 4 6 2 2 2 INDIVIDUALS % Hummingbirds 1 3 8 2 (3)• o 1 o 2 Frugivores 25 28 22 64 (24) 26 40 38 28 Fruit/Insects 40 33 36 17 (35) 34 37 33 36 Insectivores 34 36 33 17 (36) 38 22 29 34 Olhers 1 o 1 o (1) 3 1 1 o o. When 450 "extra" porokeets excludod from total. 382- WUlis ot the Madeira, either up the Guaporé or corded at or near their southwestern limits in across the Serra dos Parecís trom the Gi-Para this belt, and do not occur on the Andes or in ná River (Machados) or western heaclwaters humid forests on the lower Madeira. ot the Tapajóz. Tangará da Serra matks the The analyzable avifauna of the torests southwestern limit of the known ranges of near Tangará thus seems a mixture of species most of these species, but many may possibly of humid Amazonian forests, entering primarily be tound to circle the upper Guaporé into trom the north along the east side of the Ma eastern Santa Cruz, Bolívia. I did not see deira, and southern species ot upper tropicC~I Dendrocolaptes concolor, an ant-following bird or dry forests fringing the central part of reported from the Madeira to the Xingú and Amazonia. Many species widespread In humid replaced by subspecies of D. certhia to east central Amazonia 'ieemed absent, at least in ant west, but concolor has been reported from this briet survey: Tinamus guttatus, Tinamus the upper Guaporé (Pelzeln, 1867) and probably major, Pionites /eucogaster, Gypopsitta vulturi occurs near Tangará. na, Thamnomanes saturninus, etc. The vege In contrast to the above, Hylophyfax tation is not the tall and complex forest ot poecilonota griseiventris ot Tangará is a form central Amazonia, but a torest of moderate that occurs both east and west of the Madeirêa. (rarely low) height and moderately complex Pyriglena /euconota maura, which I en structure; and the climate is marked by a long countered only in sandy low woodland near dry "winter •. Probably the mixture of centrai the Serra, is the southern representative of a ·Amazonian and peripherai-Amazonian fore~t species that crosses central Brazil in dry birds is what one could expect from the torests and extends northewestward in sub subequatorial latitude (nearly 15° S). climate tropical forests along the Andes. and vegetation. Severa! other species or distincthte sub Studies of butterflies have also indicated species show the same pattern as that for a mixture of Peruvian-Bolivian (upper tropical), most ant-following birds, being birds from east Xingú-Tapajóz (dry forest). and central Amazo of the Madeira River: Selenidera maculirostris nian forms, but without strong restriction to gouldii, Pterog/ossus i. inscriptus, P. bitorqua Amazonian forms from east ot the Madeira; tus sturmii, and Pipra nattereri. Some species the Madeira seems less important as a ba~rier (like Pyriglena leuconota) descend along for butterflies than for birds (Brown, 1972: 191 the lower Andes and are known to extend and pers. comm.). Buttertlies show some eastward in dry forests into this ragion or endemic forms, suggesting to Brown a former beyond, but are absent from west ot the lower forest "refuge" in the region during dry Madeira: Tinamus tao, Phaethornis hispidus, climatic periods, but the avifauna seems a Aratinga weddellii, Nyctiphrynus oce/latus, mixture-as of recolonization after a dry epoch. Nystalus strio/atus, Piculus leucolaemus, Dry Haffer (1969, 1974) does not indicate that the mophila devi/lei, Herpsilochmus rufimargina region was an important refuge or center of tus, Myrmeciza hemimelaena, Tangara cyani speciation for birds. lt is possible. however, col/is, T. nigrocincta, and perhaps others. that further west along the Serra dos Parecís are better torests and better avifaunas-certain Certain species of the region ot Tan ly the butterfly fauna is richer (K. S. Brown. gará da Serra seem species of the gallery pers. comm.). woodlands and dry-forested belt extending from east of the Tapajóz River acmss into eastern Bolívia, even though the belt seems DISCUSSION interrupted by such large areas of open vege tation as the top of the Serra dos Parecis. Ara In the context of the "peripheral" (to the maracana, Ara nobilis, Brachyga/ba lugubris, Amazonian "center ") nature ot this avi fauna Captto dayi, Herpsilochmus longirostris, Neo and forest, the obgervations of birds during pe/ma pal/escens, Odontorchilus cinereus, and the cold wave <;uggest some phenomena possibly Hylophilus pectoralis are here re- which, amplified even more peripherally by Effects or a cold wavc. - 383 more frequent or stronger cold, might lead to peripherally (Table 3 compares passerines of replacement of suboscine Passeriform birds by a forest near Manaus with forest~ near Tanga oscines in those more peripheral zones. lnsec rã and with a forest even further south in São tlvorous birds became less conspicuoun during Paulo) -- whether the low vegetation is due the cold wave, while frugivorous and om to seasonal flooding (várzeas). droughts nivorous ones remained relatively consp!cuous. (caatingas, desert scrubs), cold (subtropical This suggests that insectivorous birds had forests). humans (capoeira; Novaes, 1973). or difficulties finding prey, and had no time or other reasons. The Cotingidae and Pipridae. extra energy for singing or the like; and that which are primarily fruit eaters, also occur in frugivores and omnivores moved to fruiting good numbers in or near the edges of tall trees where food remained available despite Amazonian forests, as do many frUit-eating the cold. The decreased insect activity was nonpasseriform birds (Tinamidae, Cracidae, obvious even to an ornithologist, and was Psittacidae, etc.). lt seems that, under the confirmed by entomologists in our party (K. S. relatively constant condltions of central Ama Brown, Jr.; Mohamed Habib). Fruit, by contrast. zonia, specialists either on insects (fumarioid comes from larga and resistant organisms, suboscines) or fruits (birds in the last which do not become unavailable in such brief sentence) are favored. Slightly further pe fluctuations as a cold wave (or do so only after ripherally, occasional cold waves or other the wave has passed. Observations in central • disasters" increasingly make specialized São Paulo state and in lguaçú National Park insectivores vulnerable, and they are replaced after the cold wave indicated that many trees by generalized omn!vores that can swi1ch back lost leaves, and that a few were killed). and forth between insects and fruit. In terms of avifaunas, the difficulties of The contrast between central and peri insectivores in extreme weather are significant pheral Amazonian distributions of furnarioid because a large group of suboscines, the suboscines and other passeriforms thus is furnarioid suboscines (families Formicariidae, likely to have at least one ecological basis, Furnariidae, Dendrocolaptidae), are essentially that ot occasional disasters which cauc;e difft insectivorous (Appendix). Tyranno:d sub culties for insectivores. Table 4 compares oscines (Cotingidae. Pipridae, Tyrannidae) and numbers of species of insectivores, omnivores, oscines (Hirundinidae and following families and frugivores near Manaus (3° S). Tangará in the appendix), by contrast, are mostly om (15° S), and in São Paulo (23° S), showing the nivores, rummage in protected places for food, lower percentage of species of pure insec or can migrate In unfavorable periods. In tivores near Tangará. Some individual insec general. furnarioid subosclnes dominate in tall tivores may be killed outright, at least in Amazonian forests and tyrannoids and oscines regions where cold waves or other disasters take over in any slightly lower vegetation are more frequent and stronger than at Tanga- TABLE 3 Percentages of Species of Passerine Birds in Foresta Furnarloids (%) Tyrannoids Osc ines Total n.o specles 1. Manausb: Reserva Ducke 41 35 24 130 2. Tangará Region 34 33 33 149 3 Barreiro Ricoc 33 37 30 82 o. Eucludes Corvidoe, Hirundinidoe flylng over ar neor foresls, os wcll os nonforest species cosuolly oi forcst edges. b. From Willis, ms; mlgronts ond nonforest species excludod. c. Fazendo neor Anhembf (Sõo Paulo Stote); currently under study; migronts cxcludcd. 384- Willls rá da Serra. Others may have difficulties unpredictably bad o r semiopen "ring" of reproducing in short disaster-free periods habitats has generalists, and the ccnstantly available in some years (see Willis, 1974). unfavorable and more open second "ring" of Fruit and insect eaters, however. af~ more habitats has specialists again? local lists of likely to survive brief cold waves, or can use the type here, from a wide variety of places fruits for adults while feeding insects to and habitats, might show if thi~ is indeed a nestlings, thus increasing the number of young rule of wide applicability. they can produce in short nesting seasons. The ornithologist must ask the additional Fruit eaters also have the advantage of greater question: why there is a correlation between mobility, allow1ng movements to better sites, major groups of passerines and their food than do the generally territorial or semiterri types? Was there no selection for fruit-eating torial insectivores. However, fruit eaters have furnarioids, which could thus have occupied to turn to insects, or move about, in "ha!·d niches now occupied by tyrannoids and times for fruits (Morton, 1973). oscines? Why is there no furr.arioid or ty ft One finds a rise in insectivorous speci€s rannoid that eats seeds? The oscines that eat rather than a continued decrease as one goes seeds mostly live in lower or more open even further from tall Amazonian forests, ini.:o habitats of the "second ring ", and hence h ave the "ring '' of habit~ls beyond the "peritropical not been considered above except in the list ring ''. (The data from São Paulo in Tables 3 of birds of open areas in the region of Tangará and 4 provide an example). Furnariidae and da Serra; but they and the suboscines that do Parulidae, plus a number of insectivorous not eat seeds add odd distortions to the Tyrannidae, occur out in wide open or semiope:n generally accepted or "conventional" view of zones or in temperate-zone forests. The evolution of neotropical passerines. explanation here, as far as my own obser The conventional view is that neotropi vations go, seems not so much that fruits are cal suboscines (especially the "an:estral" rare (being replaced by seeds) but that many furnarioids) are primitive forms that have been of these bird species are migratory, eat insects retreating into tropical forests ever since the in enclosed places, or have other ways of Pliocene closure of the Panamanian land avoiding bad periods, which are so common bridge allowed oscines to flood south (Amadon. as to be predictable. Closer to ta li Amazonian 1973). Some authors (Siud, 1960; Willis, 1966) forests, these species are probabiy at a disad have indicated doubts about a theory that vantage in direct competition with insectivores requires oscines not to fly over water cmd that which specialize and stay on territories (Willis, requires extensive flow of species from 1966). in the long periods between d1sasters species-poor habitats (open ones; Central and or hard times. North America) to species-rich ones (forested: Perhaps the constantly favorable "tropical South America). but the oddities of food types rain forest" has specialized birds, the next raise further doubts. In ecology, major niches 'fABLE 4 Percentages of Species o f Different Foo.:l Types in Forests• lnsectivores (%) Omnivores Frugivores Total n.o species 1. Manausb 59 30 11 183 2. Tangará 50 40 10 208 3. Barreiro Ricoc 54 36 10 115 " o t'xcludcs Apodidoe, Trochílidoe, Corvidoc, H~tu:"ldinodoe, ccrnivorcs other thon onscct veres, cnd long-dostcnce mogronts. b. From Willls, ms, nonforest specocs excludcd. c. From unpublishcd studies ín progress summering migrcnts excluded os ore wintcrlng oncs. Effects of a cold wavc ... -385 are rarely left unfilled for long; but the con that they have moved recently into the New. ventional theory seems to require unfilled (by Reversing the direction of fringillid (and hence birds) fruit-eating niches prior to tyrannoid nine-primaried oscine) movement almost elimi appearance, plus ur.filled seed-eating niches nates the supposed recent movement of until the Pliocene. oscines into the neotropics. Wrens, mimids, thrushes, and jays are small groups that may I would like '!"o suggest an alternative possibility for evolution of major groups of have moved in after closure of land bridge~ in the Pliocene, as suggested by Amadon. neotropical passerines: that suboscines that took to eating insects in closed neotropical I agree with Keast ( 1972) that there was habitats became furnarioids, related birds that probably not much movement intt' South earlier took to fruit-insect use in lower vege America prior to the Pliocene, thus leaving tation (in both New and Old World) became nine-primaried oscines and suboscines (es various suboscines, including tyrannoids, while pecially tyrannoic!s) free to radiate; but those early passerines that took to various suggest that one entrance early led to the types of feeding (including seed eating) in huge nine-primaried radiation. open areas became oscines. To use open Cracraft (1973) follows Keast and earlier habitats, a complex song and hence complex authors (Mayr, 1964) in suggesting that nine syringeal musculature are advantageous (Mor -primaried oscine::; arose in tropical North ton, 1975). lt is possible that, in intermediate America, or that the most primitive ones habitats, the variably simple to intermediate (vireos, warblers) did so, even though most syringes of tyrannoids are sufficient; and that groups are South American. Considering that in closed habitats. the peculiar "tracheophone" syringes of furnarioids produce greater volume (a) South America is likely to have been southeast of North America throughout the even i f less modulation. Migrations, pointed Cenozoic; (b) nine-primaried passerines are or nine-primaried wings, and many other open -country adaptations of oscines are not neces adapted for long-distance flights (Averill, 1925) sarlly advances over furnarioides; just neces it seems likely that (c) some migrating nine sary given an open-country environment for -primaried birds would have flown over water oscines. to or from South America and radiated southward almost as quickly as they did The alternative view would suggest that northward. Thus, evolution of nine-primaried oscines were prcsent long ago in the New oscines in North America until the Pliocene, World, and that their competition prevented followed by their flooding southward, still development of seed-eating suboscines there seems unlikely. A northward direction of as in the Old World. Separation of oscines by dispersai, from South to North America, is less continental drift in late Cretaceous or entry into South America by waif dispersai by the likely because fewer southern forms migrate Oligocene are possible, sínce Primates and well northward. However, survival of certa in rodents somehow got to South America by primitive migratory nine-primaried oscines the Oligocene (Simpson, 1969), and since mainly in North America could have resulted Brodkorb ( 1960) suggests that seeds led to from relative lack of competition from sub blrd evolution in the Miocene. New World osclnes, rather than from radlation there. Cox seedeaters (Fringillidae sensu lato, including (1968) has suggested that these migrants Emberizinae and Cardinalinae) could have are mainly ones that were interspecifically reinvaded the Old World, explaining why there outcompeted toward the equator; if so, the are two main groups of seedeating Oscines drift of continents raises anew the • southern (Fringillidae; and Ploceidae of the Old World). ancestral home" theory in an ecological The nearest relatives of Fringillidae are nine version for these migrants, with the twist that -primaried tanagers and other New-World they would have been avoiding a highly de birds, and I think it more likely that Fringillidae veloped and competitive avifauna by migrating have moved recently into the Old World than northward across the Panamá gap. 386- Willis lt does not seem likely, under e!ther the each region seem primitiva (as the lyrebirds conventional or alternate views. that nine of Australia and the Acanthisittidae of New ·primaried and other oscines originated sepa Zealand). suggesting derivativas of oscines rately in Old and New Worlds. lt is true that present before continental drift. Absence of Sibley (1970) suggests wrens show re suboscines in New Zealand and Australia semblances to furnariids in egg-white proteins. could be due to their extinction or failure to lt also is interesting that the clambering reach adversely open environments there. behavior and plush crown of the oscine rather than an indication that subosclnes arose Catablyrhynchus diadematus suggest the after separation of Australia. furnariid Metopothryx aurantiacus, while the Oscines seem unlikely to have descended clambering furna1 iid Xenerpestes minlosi from birds presently called "suboscines •• looks like a leaf-clinging Parulid. However. which have a bony stapes differwt from that Sibley indicates resemblarce of egg-white of other Aves and from Reptilia (Ft::duccia, proteins between nine-primaried oscines and 1974, 1976). "Suboscines", with thelr variable severa I Old-World groups. These and thP. syringes (Ames. 1971) could easily have similarities of oscine syringes in general descended from primitiva oscines, before or (Ames. 1971) throw doubt on separate origin as the latter developed their complex syringes. of nine-primaried oscines from local sub Possibly, to avoid confusion, the "suboscínes" oscines; it seems more likely that oscines with the modified stapes should in future had a common origin and were separated by works be given a noncommittal name like continental drift or immigrated early to South "paraoscínes ". re<>erving the name "sub America. oscines" for fossil early passerines of simple Under both thc conventlonal and alterna syringes and primitiva stapes. tive view. suboscines have been unsuccessful in the Old World. Whether they were ever ACKNOWLEDGEMENTS common there is not clear; but the presence of Eurylaimidae in Africa and Asia and of appreciate the support of the Universi Philepittidae in Madagascar indicates that dade Estadual de Campinas for the expedition suboscines evolvcd before continental drift. and the aid of other members of the group. The small size and historical vagarias of especially Keith S. Brown. Jr. . W. Be!lson. K. Old-World tropical forests could have given Brown. D. Pearson. E. Eisenmann and Yoshika the advantage to forest-edge oscines over Oniki helped with the manuscript. forest-living suboscines. The absence of furnarioíds from the Old World, h.Jwever, índicates that this group may well have SUMÁRIO evolved in the New World after Africa separated from South America. perhaps from As aves das matas do rio Sopotuba, Mato Grosso, foram estudadas durante uma "friagem" no mês tyrannoid ancestors (Sibley, 1970, doubts that de julho de 1975. As aves insetivoras foram menos Old-World suboscines are tyrannoids; if he is conspícuas e as aves frugivoras mais conspicuas right, tyrannoids and furnarioids could both durante a "friagem". É possivel que em "desastres" postdate drift). ocasionais como 3 "friagem", nas margens de flo restas tropicais, haja seleção contra aves insetivo· The ancient or pre-continental drift nature ras e seleção favorecendo as aves "onívoras", isLo of oscines is possible but uncertain under é, que comem insetos e frutas. A tendência para s~ both the alternative and conventlonal views. ter menos Passeriformes "subosclnes" nas margens Oscines occur on Madagascar, in Australia, de florestas neotropicais parece ser devido à falta and in New Zealand. three areas much more de suboscines do grupo de "furnarioides,, que são insetívoros. As teorias de que os suboscines são isolated than is South America. Some could ancestrais de "oscines", e que os oscines entraram have wandered from nearby continents, for na América do Sul no Plioceno, parecem imprová open country oscines are usually good fliers veis, pois se assim fosse, teria faltado oscines co and cross water gaps easily; but orhers in mendo sementes por várias épocas geológicas. Effects or a cold wave ... - 387 LITERAT URE CIT.ED Dobzhansky, T., M.K. Hecbt, and W. C. Steere, Evolutionary Biology, vol. 5. AMAOON, D. Appleton-Century-Crofts, N. Y. 1973 - Birds of the Congo and Amazon forests: LlSBÔA, p. L. a comparison. pp. 267·277. In Meggers. 1975 - Estudos sobre a vegetação das campi B.J., E.S. Ayensu, and W.D. Duckworth, nas A.nazônicas - II. Observ:lções ge Tropical F~rest Ecosystems in Africa rais e revisão bibliográfica sobre as and Soutb Amcrlca: a Comparative campinas Amazônicas de areia branca. Review. Smithsonian Inst. Press, Was Acta Amazonica, 5: 211-223. hington. MAYR, E. 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