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T H E C 0 N D 0 R r : : ,‘ “; i‘ . .. \ :i A JOURNAL OF AVIAN BIOLOGY ,I : Volume 99 Number 2 ’ I_ pg$$ij ,-

The Condor 99~253-270 D The Cooper Ornithological Society 1997

ON THE ORIGIN AND OF BUILDING BY ’

NICHOLAS E. COLLIAS Departmentof Biology, Universityof California, Los Angeles, CA 90024-1606

Abstract. The object of this review is to relate nest-buildingbehavior to the origin and early evolution of passerinebirds ( Passeriformes).I present evidence for the hypoth- esis that the combinationof small body size and the ability to place a constructednest where the chooses,helped make possiblea vast amountof adaptiveradiation. A great diversity of potential habitats especially accessibleto small birds was created in the late Tertiary by global climatic changes and by the continuing great evolutionary expansion of flowering plants and .Cavity or hole (in ground or ), open-cupnests (outside of holes), and domed nests (with a constructedroof) were all present very early in evolution of the Passeriformes,as indicated by the presenceof all three of these basic nest types among the most primitive families of living passerinebirds. Secondary specializationsof these basic nest types are illustratedin the largest and most successfulfamilies of suboscinebirds. Nest site and nest form and structureoften help characterizethe , as is exemplified in the suboscinesby the (Furnariidae), a large that builds among the most diverse nests of any family of birds. The domed nest is much more common among passerinesthan in non-,and it is especially frequent among the very smallestpasserine birds the world over. Each basic type of nest built by passerineshas advantagesand disadvantages in specific ecological situations,and nest type dependson a balance of multiple factors that involve the nest site, the physical environment, the community, and the size and behavior of the birds. Key words: evolution,nest, Passeriformes,body size, Furnariidae, Asthenesanthoides, auricularis.

INTRODUCTION sequent specializations of these basic nest types This review attempts to determine how nest in the evolution of the larger, more successful building relates to the origin and early evolution phylogenetic lineages of suboscine birds? (4) of a major taxonomic category-the passerine what selection pressures and ecological condi- birds. The Order Passeriformes includes three- tions led to the evolutionary origins of the basic fifths of the living of birds, and the or- nests types among passerine birds? The four igin and adaptive radiation of passerine birds is main sections of this review paper correspond to arguably the most important problem in omi- these four questions. thology, after the themselves. On the basis of various derived traits, Raikow More explicitly, the goals of this review are (1982) presents evidence that the Order - to attempt to answer four inter-related questions: iformes is a monophyletic group. The perching (1) what are the most general or basic nest types foot of passerines, unlike that of other birds, has among present-day passerine birds? (2) what a large hind whose tendon is not joined to were the basic nest types among ancestral or ear- the tendons of other , thus permitting max- ly passerines? (3) what was the history and sub- imum flexibility of the large and opposable hind toe. It is a reasonable assumption that this ar- ’ Received 7 January 1996. Accepted 24 January rangement should help many passerines in es- 1997. caping from enemies by moving speedily and

W31 254 NICHOLAS E. COLLIAS skillfully inside bushes and other dense vegeta- rensmeyer et al. 1992) and insects (Labadeira tion where they often nest. This does not ex- and Sepkoski 1993), and a great diversity and clude other possible functions of the hind toe. abundance of passerinebirds. from flow- Passeriformes share other very important an- ers and small seeds are especially available to cestral traits that are not unique to this order. small birds, while insects were probably the ma- Two of these traits that may well be keys to their jor food of early passerinesjudging from prim- successin evolution are small body size (Fitz- itive passerinestoday. patrick 1988, Kochmer and Wagner 1988) and A theoretical basis for the evolution of the the building of elaborate nests (Collias and Col- Order Passeriformes as a major taxonomic cat- lias 1984). Since passerine birds are in general egory stems from the book by Simpson (1944) smaller than birds of most other orders, and in- Tempo and Mode in Evolution, and his later clude more species than all other orders com- book (1953) on The Mujor Features of Evolu- bined, it is clear that passerine birds have gen- tion where he states(p. 346): “As a generaliza- erally done better than larger birds in invading tion, the development of a higher category the diverse terrestrial habitats of the earth. seems always to involve the rise of some dis- Small body size may not be the only trait re- tinctive sort of related to spread into sponsible for success of passerine birds. Fitz- a major adaptive zone.” Simpson deduced cer- patrick (1988:75) states: “some aspectsof being tain broad principles of evolution from the best small-bodied, large-brained, arboreal, diurnal, known histories of , especially largely insectivorous, with high metabolic rate, . He recognizes three modes or phases short generation time, and vocally sophisticated in the evolution of a major taxonomic category. appear to have endowed members of the passer- I apply these three phasesto the evolution of the ine with the opportunity or propensity to Passeriformesin an attempt to interpret the early radiate at a rate faster than that characterizing evolution of nest building by passerine birds. birds of any other clade.” To this list, I would These three phasesare about as follows: add and emphasize passerine nest-building be- havior. NEW ECOLOGICAL OPPORTUNITIES In general, small body size combined with A vast number of new ecological niches in the powers of flight has important implications for Late Tertiary must have opened up with the nest-building behavior. Small birds often build greatly increased environmental and biotic di- relatively small nests that can be placed and hid- versification over the world (Behrensmeyer et al. den in a great variety of nest sites by different 1992). Early passerine birds were uniquely pre- species. Small birds can build with lighter ma- adapted to invade many such new habitats by terials and may thus reduce the energetic costs their small body size, powers of flight, and flex- of building. ible nesting behavior. The ability of passerine Most modern orders of birds seem to have birds to construct their nests where they wish arisen in the early Tertiary, but fossil passerine must have greatly increased the number and va- birds do not appear in large numbers until the riety of nest sites available to them, enabling late Cenozoic (Olson 1989, Fedducia 1995). The them to compete effectively with the hole-nest- Passeriformes were not important components ing and often larger coraciiform and piciform of the avian fauna until the . The pre- birds (Collias 1964). Numerous nest sites, more viously dominant arboreal perching birds were available to small than to large birds, must have the (Olson 1989, Fedducia 1995) included nesting on green land plants or on all modern representatives of which are hole- emergent green plants over water, or on twigs nesters (Collias and Collias 1984). and fine branches of bushes or , as well as The most evident environmental change nests pensile from drooping twigs or vines. world wide during the late Cenozoic has been the diminishing of and the concomitant PRIMARY ADAPTIVE RADIATION expansion of open woodlands, grasslands, and Radiation initially at the level of species and (Bebrensmeyer et al. 1992). Increased genera gives a trial and error mechanism for global diversification and seasonalityof environ- evolution. Early in evolution of primitive pas- ments was accompanied by a continuing great serines, there were three basic nest types: hole increase in diversity of flowering plants (Beh- nests (in ground or tree), nests open above, and EVOLUTION OF PASSERINE NEST BUILDING 255 domed (constructed roof) nests. Evidence for TABLE 1. Percentages of bird families with species this conclusion comes from the nests of the most having the basic nest type indicated.* Hole nests in ground or tree. Open nests (not in holes) may be a primitive living passerines(see below). cup, bowl, or platform. Domed nests have a construct- ed roof. SECONDARY ADAPTIVE RADIATION AND SPECIALIZATION Percentage of families** Number Secondary radiation and specialization involved of HoIt Open Domed famdles nest nest persistence of the more successfullines in evo- nest lution. Different phylogenetic lines (genera, sub- Non-passerine families 96 34 77 7 families and families) have elaborated different Passerine families 6.5 56 68 52 specializations of the basic nest types. Parallel Comparing suborders: and are common, especial- Suboscines 12 50 42 58 ly among passerine birds (Mayr and Ashlock Oscines 53 55 74 51 Comparing nest sites: 1991) and their nests (Collias and Collias 1984). Ground nests 27 31 41 52 Secondary adaptive diversification of nests will Nests above ground 62 44 63 48 be exemplified below with three large suboscine * For references see Hamson 1978, Colbas and Colhas 1984. Stdes families, the Tyrannidae, Thamnophilidae, and and Skutcb 1989. Also see Table 2. ** Percentages do not equal 100 because some bud families have more especially the Fumariidae. Domed nests have than one basic nest type. evolved by two routes: roofs on ground nests, and on nests in trees hung from peripheral cance of differences; df = 1 for all these tests. drooping branches, twigs and vines. Passerines nest in holes more often than non- passerines(x2 = 7.0, P < 0.01). The domed nest BASIC NEST TYPES AMONG PASSERINE is several times more frequent in passerinesthan BIRDS in non-passerines(x2 = 41.4, P < 0.001). Open Knowledge of the basic nest types setsthe stage nests are more frequent in passerinenests above for further analysis. Basic nest types refer es- the ground than on the ground (x2 = 3.8, P = pecially to nest form and general nest site, and 0.053), and open nests are much more frequent among passerinebirds include hole nests, open- in the oscines than in the suboscines(x2 = 4.56, cup nests (not in holes) and domed nests with a P = 0.03). constructed roof. Hole nests may be in the Table 1 shows that within the suboscines, ground, in rock crevices, or in trees. The reason domed nests are the most frequent nest type; but these nest types are termed “basic nest types” the number of suboscine families (12) is prob- is because each basic nest type has been elabo- ably inadequate for a statistical test. The Mc- rated in evolution into a wide variety of subsid- Nemar test (x2,J is appropriate for the same set iary and specialized kinds of nest (Collias and of families examined twice (Altman 1991); in Collias 1984). this case we asked whether each family did or Table 1 shows the frequency of the basic nest did not have an open and/or domed nest. Within types in the Passeriformes. This table is based the oscine suborder open nests (32/53 families; on the number of families having each nest type 60%) are more frequent than domed nests (20/53 (Collias and Collias 1984). It should be recog- families; 37.8%) (x~,~ = 4.23, df = 1, P = 0.04). nized that some bird families may have more Furthermore, there are 23 families of oscines than one basic nest type and may be entered into that have open but not domed nests, and only the table more than once. In general, the tax- 11 families of oscines that have domed but not onomy followed is that in the referencescited in open nests. In passerine nests above ground, the table. open nests (not in holes) are more frequent than Table 1 first comparespasserine with non-pas- nests in holes (x’,,,~ = 3.8, P = 0.05) but do not serine families. In both casesa nest open above differ from the frequency of domed nests (x’,,,~ is the most frequent type. For this table, chi- = 1.80, P = 0.18) square (x2) tests were used for comparisons of two independent groups within columns. Al- ORIGIN OF BASIC NEST TYPES IN though the table shows percentagesof different PASSERINE EVOLUTION nest type for each group, the actual nest fre- Before considering nests of the possible ances- quencies were used for calculations of signifi- tors of passerine birds, one may ask what was 256 NICHOLAS E. COLLIAS the evolutionary sequence for the basic nest Based on syringeal structure, the Order Pas- types: hole, open, or domed nest? Simpson seriformes is often divided into suboscine and (1944, 1961) and Mayr and Ashlock (1991) have oscine birds. Ames (1971) concluded that the discussedcriteria for helping to decide whether suboscines, which together with the a given trait is ancestral or derived within a giv- (Menuridae) and (Atrichomithidae) en taxonomic group. None of these criteria (e.g., have a simpler , are more primitive than generality, simplicity, , or outgroup the rest of the oscine passerines. For further comparison) is sufficient by itself. analysis of early nest evolution, I focus on the A hole nest in the ground is very common suboscinesand the lyrebirds and scrubbirds. among , the ancestral to birds, sug- There is agreement, based on both morphol- gesting that the hole nest is probably most prim- ogy (Raikow 1987) and DNA hybridization itive for birds that sit on their . Nests built (Sibley and Ahlquist 1990) combined with nu- in pre-existing holes generally lack the site flex- merical cladistic analysis (by these authors), that ibility of nests constructedin a site of the bird’s the most primitive families of the Order Passer- own choosing, because open nests and domed iformes are the nine small families listed in Ta- nests can be placed in a greater number of sites ble 2. These include seven families of suboscine above ground as well as on the ground than can passerines plus the Australian lyrebirds and hole nests. scrubbirds which often are considered to be the The open nest, by the criteria of commonality most primitive oscine passerines and are some- (general occurrence), relative simplicity, and on- times placed in a suborder of their own (Men- togeny, appears closer to the ancestral type of urae). Except for the lyrebirds, 8 of the 9 prim- than does the domed nest. We cannot itive families are generally small birds and have use the criterion of outgroup comparison with one or more speciesonly 15 cm or less in body much confidence to distinguish ancestral from length. Table 2 also showsthe number of species derived nest types for the Order Passeriformes for which nest-type data exist in each of these becausethe non-passerine order most closely re- families that builds the nest type indicated. lated to the Passeriformes is controversial, and However, there is no general agreement as to because parallelism and convergence are ram- which of these nine primitive families most pant among passerines (Mayr and Ashlock closely resembles the passerine ancestors. Pre- 1991), including their nests (Collias and Collias sumably they all share some traits of the com- 1984). mon ancestor. Evidence from bird ectoparasites,i.e., Traditionally, the broadbills () of lice (order Phthraptera;Turner 197 1) and feather tropical forests have been considered mites (Order Acarina; Cemy 1973), that have to be the most primitive living family of passer- evolved with their hosts supportsthe traditional ine birds, and they often have been listed first in view (AOU 1983) based largely on morphology classifications of passerine families (Harrison that the closest common ancestorswith the pas- 1978). Broadbills and philepittids build pensile serine order are the coraciiform and piciform or- nests with a side entrance and the nests may be ders (Collias and Collias 1984), all species of high up in trees. Prum (1993) studied the phy- which nest in holes. The ultrastructure of feath- logeny of the broadbills, and concluded that the ers (Chandler 1916, Brom 1990) supportsclose rather specialized nests were all derived within relationship of the Passeriformes to piciform the family. He also united the Eurylaimidae and birds and to . Evidence from Philepittidae into one family. DNA hybridization (Sibley and Ahlquist 1990) Sibley and Ahlquist (1990) concluded from does not support close phylogenetic relationship DNA hybridization studies that “the acanthisit- of the passerine order to the coraciiform-- tids are the survivors of an ancient passerinelin- form birds, but places the Passeriformesclosest eage with no close relatives” and that it is pos- to various open-nesting orders. It is possible that sible that they should be assignedto a third sub- the common ancestor of the passerine and relat- order as the sister group of the suboscinesand ed orders built an open nest, but the matter can- oscines. The three living species of New Zea- not be regarded as settled because of the prev- land (acanthisittids) build enclosed nests, alence of parallel and convergent evolution in often nesting in tree holes or in rock crevices. nest building. Feduccia and Olson (1982) suggestedthat the EVOLUTION OF PASSERINE NEST BUILDING 257

TABLE 2. Basic nest types within the most primitive families of passerinebirds. Number of species having each nest type are tabulated (some species have more than one nest type). Number of species examined per family in parenthesis.

Nest on ground Nest above ground Family (n species) I” burrow and reference no.* or crevice Domed Open In tree hole Domed Ope” Acanthisittidae(3) 1 3 2 2 Atrichornithidae (2) 2 2 Menuridae (2) 2 2 1 1 Pittidae (12) 3,4 9 1 I Philepittidae (2) 5 2 pensile Eurylaimidae (10) 3 10 pensile (8) 6 (ground ) 3 I Conopophagidae(2) 7 1 2 Rhinocryptidae (14) 8 12 1 3 2 Total (55 species) 15 14 1 10 24 9

* 1(Oliver 1955, Falla et al. 1978). 2 (Frith 1979). 3 (Medway and Wells 1976, Smythies and Cranbrook 1981, Ali and Ripley 1983, Keith et al. 1992). 4 (Co&es 1990). 5 (Langrand 1990). 6 (Wiedenfeld 1984, Hilty and Brown 1986, Qumtela 1987, Stiles and Skutch 1989, Whitney 1992, Ridgely and Tudor 1994), 7 (Fraga and Narosky 1985, Hdty and Brown 1986). 8 (Johnson and Goodall 1967. Stiles 1979, Fraga and Narosky 1985, H&y and Brown 1986, Rosenberg 1986).

Australian lyrebirds (Menuridae) and scrubbirds types: hole (ground or tree-hole), open, and (Atrichomithidae) together with the domed nests. Thus passerinebirds probably built (Rhinocryptidae) “are among the most all the basic nest types very early in their evo- primitive of the Passeriformes and are represen- lution, even though the very first ancestorof the tative of the ancestral stock that gave rise to the Order Passeriformes and its nest form remains remainder of the passerines.” But Rich et al. uncertain. (1985) attributed some of the skeletal similari- If all nine primitive passerine families are ties between these groups to convergence re- consideredtogether, Table 2 brings out this same sulting from weak powers of flight. Birds of point somewhat differently. Hole-nesters include these families build enclosed nests, the Austra- 25 speciesin five families, birds with open nests lian specieson or just above the ground, where- include 10 species in two families, while birds as the tapaculosbuild a variety of hole or domed with domed nests include 38 species in seven nests and many of the species nest in burrows families. Compared with passerinebirds in gen- or rock crevices. eral (Table l), there seems to be a smaller per- Ames (1971) and Fedducia and Olson (1982) centage of open nests in the primitive families. described certain primitive characteristicsof the However, the main point is again, that all the ground antbirds (, , and basic nest types are present among primitive liv- their allies), Formicariidae in the narrow sense ing passerines, suggesting a similar range of of Sibley and Ahlquist (1990), and the allied adaptability in nest-building behavior of early (Conopophagidae). These traits agree passerine birds. with the DNA hybridization results of Sibley Table 2 also shows that primitive passerine and Ahlquist (1990). Helmut Sick (1993:394) families taken together often build their nests states that “Various indications lead me to be- above the ground (43 species in all nine primi- lieve that the oldest Passerines were terrestrial tive families), and also fairly often in or on the resembling formicariids such as the Grallaria ground (30 species in five families). This sug- .” The ground antbirds and the gnatea- geststhat early passerineshad considerable flex- ters generally have open-cup or open-bowl ibility in choice of nest sites. nests, unlike the other primitive families of sub- Six of the nine primitive passerine families oscines which have hole or domed nests (Table have more than one of the basic nest types and 2). nest sites (Table 2), suggesting adaptive flexi- To recapitulate, the four or five families each bility within as well as between these families. considered by different authorities to be the In fact, in three of these families, the same spe- most primitive passerine family or families, cies may build on the ground or above the when taken together build all the basic nest ground, in holes or outside holes, including the 258 NICHOLAS E. COLLIAS

Rifleman (Acanthisittu chloris; Gray 1969), the generic levels in the passerineorder (Collias and Superb (Menura novaehollandiae) and Collias 1984). the Noisy (Pitta versicolor) (Frith 1979). The Tyrannidae is one of the largest bird fam- The (P. iris) helps bridge the gap ilies in the world (Stiles and Skutch 1989). Tray- between two basic nest types; it builds a domed lor and Fitzpatrick (1982) tabulated the nests of nest varying to a shallower, partly open nest on the many genera. Nest form is generally consis- the ground or up to 3 m above ground. tent for different species in the same genus. In conclusion, the nine most primitive passer- There are about twice as many genera with an ine families, taken together, have all the basic open-cup nest (60%) as with a domed (not in a nest types of passerine birds: hole nests (in hole) nest (31%), whereas nests in holes (10%) ground or tree-holes), open-cup or open-bowl are much less frequent. nests (outside of holes), and domed nests with a Traylor and Fitzpatrick (1982) place the genus constructedroof. If these nine primitive families Eluenia (cup nest) as most primitive in the fam- and their varied nests are representative of early ily. Based on phylogenetic studies of many tyr- passerinebirds, one can conclude that such pas- anmd groups, cup nests have apparently evolved serines were pre-adapted by their nest diversity independently and repeatedly into globular for invasion and specialization into a great va- (domed) nests in New World flycatchers (Prum riety of nest sites. The primary adaptive radia- and Lanyon 1989). In Helmut Sick’s general ac- tion of species and their nests in the primitive count of the Tyramridae, he states “Many spe- passerine families fits into Simpson’s (1944) cies with closed nests . . have colored eggs, general picture of the initial “explosive” adap- demonstrating their descent from ancestorswith tive radiation of a major taxonomic group, here open nests” (1993:458). Fitzpatrick has seen the the Order Passeriformes. (Pitangus sulphuratus) “build- ing a perfectly normal open cup, which it then EVOLUTION OF INCREASED NEST gradually covered over during the first two DIVERSITY WITHIN LARGE weeks of incubation” (Traylor and Fitzpatrick SUBOSCINE FAMILIES 1982: 16). All this evidence suggeststhat the im- The object of this section is to illustrate second- mediate ancestorsof the Tyrannidae built open- ary adaptive radiation and specialization of nests cup nests. within the largest and most successfulsuboscine Based on results with DNA hybridization, families, the New World flycatchers (Tyramri- Sibley and Ahlquist (1985) recognized a lineage dae, 384 species, Stiles and Skutch 1989), typi- of tyrannids which separatedfrom the other tyr- cal antbirds (Thamnophilidae, 188 species, Sib- anmds before the radiation of the typical tyrants, ley and Ahlquist 1990), and ovenbirds (Fuma- , , and began. They riidae, 214 species,Stiles and Skutch 1989). The designated this group the subfamily Pipromor- Tyrannidae and the Fumariidae build among the phinae and considered it to be the sister group most diverse nests of any family of birds. of the other subfamilies of Tyrannidae. They The preceding section showed how primary suggestthat the Pipromorphinae may include at adaptive radiation of nests, illustrated by primi- least eight genera. Of these eight genera, infor- tive passerine families, helped to lay the basis mation on the nest is available for six: for expansion of the passerineorder. The present (including Pipromorpha), , Pseudo- section illustrates how secondary adaptive radi- triccus, Corythopis, , and Todiros- ation and diversification within large suboscine trum. Insofar as it is known, all of these six gen- families leads to multiplication of genera with era build domed (roofed) nests. Considering the characteristic nests, especially exemplified by frequency of parallel and convergent evolution the ovenbirds. Nest form and structure often of nests in the Tyrannidae, it still is possible that help to characterize genera in birds (Collias and the common ancestor of this family built an Collias 1984). About half (48%) of 65 passerine open-cup nest and that the pipromorphs inde- families have more than one of the basic nest pendently evolved domed nests. types (hole, open, or domed) compared with Within the Tyrannidae, many specialized sub- only about 16% of 96 non-passerine families (x2 types of cup and domed nests have evolved; = 19.5, P < O.OOl), suggestingmore active evo- these are described by Skutch (1960), and by lution of nest-building behavior at subfamily and Hilty and Brown (1986). For example, the open- EVOLUTION OF PASSERINE NEST BUILDING 259 cup nest in different species and genera may a roof. The Bay-capped -Spinetail (Spar- vary greatly in depth, mode of attachment to the tonoica maluroides) builds a more or less open substrate, thickness of walls, compactness or nest on or very close to the ground amidst dense looseness, and in nature of the nest materials clumps of rushes (S&pus) and grasses (Ziza- used. In this family, open-cup nests may often niopsis) that effectively roof over the nest (Na- be saddled on a branch or suspendedby the rim, rosky 1973). whereas domed nests in trees or bushes gener- Cladistic analysis of genera by Fitz- ally are pensile. patrick (1982) based on Vaurie’s 1980 mono- Besides the tyrant flycatchers and the oven- graph indicates certain genera as the outgroups birds, the largest family of New World subo- to the rest of the Fumariidae. Omitting the high- seines is the typical antbirds (Thamnophilidae). ly specialized adobe nests of homeros (Furnar- Like the tyrant flycatchers, their center of abun- ius), this analysis suggests that ground-hole dance is the lowland . The fam- nesters, such as the miners () which ex- ily has specialized on variations on the open-cup cavate and nest in tunnels, are closest to the an- nest. The typical antbirds parallel many tyrant cestral type. But DNA hybridization studies of flycatchersin similar specializations of the open- the ovenbirds indicated the leaftossers (Scleru- cup nest which, as in nests of the tyrant flycatch- rus) as the sister group to the rest of the oven- ers, varies with different species in depth, at- birds (Sibley and Ahlquist 1990). Leaftossers, tachment, thickness, compactnessor looseness, like miners, also excavate a tunnel in for and in nature of nest materials, as described by their nests, which also suggeststhat nesting in Skutch (1969a, 1996), Hilty and Brown (1986) holes in the ground was the primitive nest type and Stiles and Skutch (1989). These particular in Fumariidae. There is an interesting parallel convergences in the two different families sug- with an oscine family, the (Hirundin- gest specific selection pressuresthat remain to idae), which also has diverse nests and in which be investigated. For example, many of the typ- a phylogenetic analysis suggestedthat digging a ical antbirds, like some flycatchers, have open- burrow was the primitive nest type (Winkler and cup nests suspendedby the rim in a twig fork, Sheldon 1993). but the adaptive significance of this mode of at- Nests of Furnariidae, insofar as then known, tachment is unknown. Rarely, thamnophilid - were described by Vaurie (1980). Other impor- birds place the nest in a hollow stump (Bicol- tant general descriptions of furnariid nests are ored Antbird bicolor) or build a by Hudson (1920), Johnsonand Goodall (1967), domed nest in a bush as by the tiny Brown-bel- Skutch (1969a, 1996), Hilty and Brown (1986), lied Antwren gutturalis or by the Stiles and Skutch (1989) Sick (1993), and Rid- White-backed Fire-eye Pyriglena leuconota gely and Tudor (1994). A very useful book by which places its domed nest on or near the Narosky et al. (1983) describesnests of the Fur- ground in herbaceous vegetation (Oniki 1979, nariidae of , where 76 speciesof oven- Sick 1993). birds have been recorded (Narosky and Yzurieta The ovenbirds (Furnariidae) will be used here (1987). In Argentina during the southern spring to exemplify secondary adaptive radiation of 1989, I saw examples of most of the main among enclosed nests. Virtually all fumariids, as types of fumariid nests. far as we know, have enclosed nests, either in a Table 3 lists the main types of nests built burrow, rock crevice, tree hole, or other pro- within different genera of the ovenbirds. This tected place, or else construct their own roof, so table is based on 116 speciesand 3 1 genera with fumariid ancestors must have built enclosed adequate information on the nest, out of 214 nests. Only two fumariids have been described species and 34 genera of Furnariidae listed by as having an open nest. The Band-tailed Homer0 Vaurie (1980) in his monograph of the family. (Furnarius jigulus) does not build the adobe Information on the nest of more speciesof oven- oven nest typical of its genus, but makes a sim- birds probably would not radically change the ple, open nest of grass in a well-protected place, general picture because general nest form and e.g., beneath roof tiles, hidden among epiphytic structure is usually characteristicof the genus in bromeliads, or among bases of large, erect palm passerinebirds (Collias and Collias 1984). Vau- (Studer and Veilliard 1990, Sick 1993). It rie combined many old monotypic genera into is evident that such nest sites in effect provide fewer genera, resulting in considerabletaxonom- 260 NICHOLAS E. COLLIAS

TABLE 3. Nests of ovenbirds, Fumariidae; summary table for genera. Number of species per genus with adequateinformation on nest in parenthesis.Some speciesbuild in more than one type of nest site.

Nest on eround Nest above mound

In burrow or crevice Domed Open In free hole Domed Open Geosittu (7) and (9) 16 (7) 7 Chilia (1) 1 Furnan’us (4) 1 (rare) 3 adobe l* Eremobius (1) 1 Aphrusruru (1) Spartonoicu (1) 1* Limnornis(2) 2 woven Phleocryptes (1) 1 woven (1) 1 Leptusthenura (5) 2 I 2 4 Schizoeacu(2) 2 mossy Schoeniophylux(1) 1 Certhiuxis(2) and Crunioleucu(8) 10 Synulluxis(12) 2 11 Asrhenes (13) 1 5 1 5** Coryphisturu(1) 1** Anumbius(1) 1** (7) 7 Pseudoseisuru (3) 3 Marguromis (1) 1 mossy Pseudocolapres (2) 2 (7) 2 6 (5), (3) and Thripudectes (3) 11 (saucer lining) Lochmius (1) 1 (globular lining) Pygurrhichas (1) and (3) 4 Total: 116 species(31 genera) 41 (11) 10 (5) 0 19 (10) 53 (16) 2 (2)

* F. ~?gulus (Sick 1993). S. maluroides (Narosky 1973). **Asthma baeri, Co~phistura, and Anumbias with narrow superior entrance tunnel to chamber in thick, oval nests.

ic simplification, although further study may be types of nests built in the Furnariidae. The im- needed in some cases (Fitzpatrick 1982). pressive diversity of enclosed nests built in this Table 3 shows that, in general, the type of family is evident. Figures l-3 illustrate three of furnariid nest helps characterize and is usually the most distinctive nest types. consistent with the genus. Genera are defined by Some species and a few genera of ovenbirds several characters(Mayr and Ashlock 1991), of vary greatly in their nest building, which might which the nest is only one, but a very helpful suggesthow one kind of nest may have evolved one. Of 19 genera in Table 3 with more than one into another. Some ground-nesting species (in species listed, 16 or 84% build only one basic Geositta, Cinclodes, and Automolus) may dig type of nest, either a hole-nest or a domed nest. their own nest tunnel or use other holes such as Only 3 genera (Fumarius, Leptasthenura, and burrows. Treehunters (Xenops) may dig Asthenes) have more than one basic nest type their own nest hole in a tree, or use one dug by (binomial test, P = 0.002, comparing 3 genera a piculet (Picumnus). Some furnariid species versus 0 if one assumesall genera have the same may nest in holes in the ground and also in holes basic nest type). The -spinetails (Leptasther- in trees, e.g., Philydor rufus, the Buff-fronted nura) have four types of nests and nest sites, but Foliage-Gleaner. Domed nests of these birds often occupy old nests of various (spinetails) are generally built of twigs, but S. other species of birds. They characteristically albescens,the Pale-breasted Spinetail often uses line their nests heavily with . straws or grassesinstead of twigs. Domed nests Table 4 describes well-established examples of species of Asthenes may be placed on the of nests of different speciesrepresenting various ground or in bushes, whereas the nest entrance EVOLUTION OF PASSERINE NEST BUILDING 261

TABLE 4. Examples of species representing special types of ovenbird (Fumariidae) nests.

A. Hole nests I. In tunnel dug in soil, Geosirra cunicularia (): Automolus leucoprhalmus (White-eyed Foliage-Gleaner) with cup-nest of plant stems in chamber at end of tunnel; Lochmias nemarura (Sharp tailed Streamcreeper) builds globular nest of plant material with side entrance in tunnel. 2. Natural cavities in ground or tree. Cinclodes paragonicus (Dark-bellied Cinclodes) nest usually in ground: spinicaudus (Thorn-tailed Rayadito) nest usually in cavities of trees or behind piece of bark. 3. An excavated tree-hole. Pygarrhichas albogularis (White-throated Treerunner) digs its nest hole in de- caying wood. B. Domed (with constructed roof) nests with one compartment. I. Adobe nest. Funtan’us rujiis (Rufous Homero). 2. Grass nest on ground. Asthenes hudsoni (Hudson’s ). 3. Twig nest with side entrance, on bushes or trees. Pseudoseisura gurturafis (White-throated , Fig. 1); Schoeniophylax phryganophila (); Synallaxis spiri (Chicli Spinetail). 4. Mossy nest. Margaromis squamiger () nest with side entrance; Cranioleucus eryrhrops (Red-faced Spinetail) nest with bottom entrance. 5. Nest woven of flexible plant materials in aquatic vegetation. Limnomis curvirostris (Curve-billed Reed- haunter); Phleocryptes melanops (Wren-like Rushbird) nest exterior with pellets of mud or . C. Thick-walled twig nests with narrow top entrance tunnel. Anumbias annumbi (Firewood-gatherer); Coty- phistera alaudina (-like Brushrunner). D. Compound nest of twigs. Roofed pensile nest with more than one compartment. Phacellodomus ruffrons inomtus (Plain-fronted Thombird, Fig. 2). E. Uses and lines tree cavities or domed nests of another species of fumariid. Leptasrhenura plafensis (Tufted Tit-Spinetail). varies in this genus from one side to a narrow nest is occupied by only one pair of thombirds entrance tunnel opening at the top of the nest. and their young, and the eggs are laid only in Compound nests of Phacellodomus rujifrons the bottom compartment. The Greater Thombird inomarus. the Plain-fronted Thombird (Fig. 2), (P. ruber) has only one or two compartments in vary considerably in length and number of nest its large twig nest (Narosky et al. 1983). compartments, up to eight or nine that are built The different nest types of (Ashe- one above the other, each with its own side en- nes) suggest that a change from nesting in the trance (Skutch 1969b, 1996, Thomas 1983). A ground to nesting above ground in shrubs might

FIGURE I. Nest of White-throated Cacholote. 262 NICHOLAS E. COLLIAS

have evolved in this genus. Five of seven plain- backed species of Asthenes build domed nests on branches of shrubs, whereas the other two species nest either in a hole in the ground (A. modesta) or in a (A. cactorum) (Vaurie 1980, Narosky et al. 1983). Four other species of Asthenes have black-streaked upperpartsand build domed nests on the ground (Vaurie 1980, Narosky et al. 1983, Ridgely and Tudor 1994). To this list we add a fifth species,A. anthoides with black-streaked upperparts. In Patagonia we found a ground nest of A. anthoides, the , the nest site of which has not been described before. This nest is of interest because it may represent an inter- mediate stage between nesting in the ground, or above ground. The nest (Fig. 3) was found in Santa Cruz province in near the Rio Chico, southwest of the city of Rio Gallegos (approx. 52”S, 69”W). The nest was hidden on the ground just beneath the center of a low, densely branchedjuniper-like shrub. The parents brought insects to the nest bush, and on parting the dense foliage I saw the nest which was half- way in the ground. It was in a depressionin the soil about 5 cm deep that had presumably been FIGURE 2. Nest of Plain-fronted Thornbird. scraped out by the birds and which was lined with white feathers. This depression was cov- ered by a domed roof of twigs laid sparsely over some dark soft plant material, whereas sides of the entrance were of dry grass stems. The side entrance was about 5 cm in diameter. There were

FIGURE 3. Nest of Austral Canastero. EVOLUTION OF PASSERINE NEST BUILDING 263 two nestlings well down in the nest, so we did Nests in the ground may be less vulnerable to not disturb the nest further. The specieswas con- predators than nests on the surface of the firmed at the time as Asthenes anthoides by ground, as shown by controlled field experi- Steven L. Hilty and Maurice Rumboll. This spe- ments with artificial nests (Martin 1987). cies is the only canasterowith a heavily streaked eggs in a wicker basket lined with leaves and back (which we saw clearly) in that part of Ar- placed on the surface of the ground in an Ari- gentina (Narosky and Yzurieta 1987). zona had a significantly higher Johnsonand Goodall ( 1967) mention that Pas- rate than similar artificial nests buried with the sler found Asthenes anthoides nesting “among rim even with the ground and partially covered shrubs” in central , that the entrance hole with dead leaves, or eggs simply placed in a hole was close to the top of the rounded nest and in the ground. protected by a ring of twigs, and that the nest Tree-hole nests probably provide enhanced was lined with plant down, dry , and protection from and from enemies, flowers. Unfortunately, one cannot tell from this compared with ground-hole nests. Evidence also description whether the nest was on the ground, indicates tree-hole nests are safer from enemies or up in a shrub. than open nests not in holes. In central Arizona, Further progress in the analysis of the early nest successwas shown for various species to evolution of passerinenest-building comes from be higher in tree-hole nests than in open nests, comparing the ecological conditions that favor and best in tree holes that had been excavated the evolution of each nest type. by the birds ( and smaller species of )themselves (Martin and Li 1992). ECOLOGICAL CONDITIONS THAT The population density of hole-nesting birds FAVOR EVOLUTION OF THE BASIC often is limited by the availability of tree cavi- PASSERINE NESTS ties suitable for nesting, and populations of such The nests of birds, like foraging behavior pat- birds often have been increased by putting up , give clues to significant problems of ecol- nest boxes (Hogstad 1975, Bock et al. 1992). ogy (Collias and Collias 1984, Collias 1986, Nest cavities excavated by woodpeckers also 1991). In forest birds of Arizona, Martin (1988) may make it possible for hole-nesting swallows found that numbers of species were more cor- to nest in some areas (Daily et al. 1993). There related with density of nesting substratesthan are no woodpeckersin and New Guin- with foraging heights and places. ea and also relatively few passerine birds that In this section I briefly consider some of the nest in tree holes. Only 4 of 33 families (12%) adaptive advantages and disadvantages of hole in Australia (Frith 1979) and only 3 of 33 fam- (cavity) nests, open-cup nests (not in holes), and ilies (9%) in New Guinea (Coates 1990) include domed (constructed roof) nests. A more com- passerine species nesting in tree holes, much prehensive treatment is in our book on Nest fewer than is general among passerinesover the Building and Bird Behavior (Collias and Collias world (Table 1). 1984). The disadvantages of nesting in tree cavities Hole nests in general are safer and fledge include intense for tree holes with more young than do nests not in holes (reviewed other birds, as well as excessive exposure to ar- by Collias and Collias 1984, Skutch 1985). Cav- thropod nest parasites (Collias and Collias ity nesting gives shelter from the weather, helps 1984). In a nine- study in south Sweden, ameliorate temperature fluctuations, and con- Nilsson (1984) found that rate of nest failure and serves energy (Kendeigh 1961). rate of predation were greater in nest holes or Hole nests in the ground protect from wind nest boxes situated low in trees than higher up. chill. In Patagonia, ground-tyrants (Muscisuxi- High nest holes were preferred and four differ- cola, Tyrannidae) escape strong cold winds by ent speciesof passerinebirds occupied decreas- nesting in tunnels in the ground, a clear case of ing nest heights according to their dominance convergent evolution with the miners, Geositta status. (Johnson and Goodall 1967) and earthcreepers, To a considerable extent, passerinebirds prob- Upucerthia (Narosky et al. 1987). These tunnels ably were able to escape competition for nest often are placed in slopes or banks giving some holes by constructing their own nests in sites of protection from rain or floods. their own choosing other than holes (Collias 264 NICHOLAS E. COLLIAS

1964). Birds with open nests tend to avoid areas tively placed often may be advantageousto birds with a high density of birds that nest in tree breeding in the cool northern spring. holes (Hogstad 1975, Bock et al. 1992) Parallel analogous to the above Flexibility in nest site selection with a con- occur on mountains in tropical latitudes. In trees structed nest makes it possible for some species on the slopes of the Mauna Kea volcano in Ha- of birds to shift from nesting on the ground to waii, the open-cup nests of a honey creeper, the nesting in trees, and vice versa. Mountain Common Amakihi ( v. virens), White-crowned Sparrows ( leuco- were placed in sites more exposed to the sun phrys oriantha) in California usually build their during the cool early breeding period, but were open-cup nests in vegetation on the ground placed deeper in the later in the breeding where they are better protected from storms and seasonwhen the weather was warmer (van Riper wind-chill, but in of late snowfall during et al. 1993). the breeding season, many nests are placed up Construction and evolution of a roof on in willows and scrub pines (Morton et al. 1972). ground nests may be favored because predators Open-cup nests have an advantage over are generally more numerous on the ground, domed nests in that they are often made of fewer where open nests may be more subject to pre- materials and, other things being equal, should dation. In controlled experiments in lowland therefore generally take less time and energy to rainforest in , artificial wicker nests, build. This difference reaches its climax in the lined with green leaves and containing quail nests of some cotingas (Cotingidae) in tropical eggs, had significantly more predation when (Hilty and Brown 1986), certain placed on the ground than when placed 1 m and ( chloris; Pycnonotidae) in trop- 2 m up in trees. Predation rates also were greater ical (Chapin, 1953), and certain - on such artificial open-cup nests than on artifi- (Ldage leucomela; Campephagidae) of cial enclosed nests placed in similar situations Australia (Frith 1979), where the nest is so small (Loiselle and Hoppes 1983). Haskell(1995) and that it may be completely hidden by the incu- Major and Kendal(1996) in an extensive review bating bird. At the same time, very small nest of artificial nest experiments have cautioned size helps hide the nest from eyes of predators against various pitfalls in such experiments, but (Snow 1976). agree on their potential value. The open-cup nest presumably favors a quick- In and neighboring countries, 68% of 19 er escape from the attack of a predator, freeing species of babblers (Timaliidae) that build their the bird to breed again if its nest is predated. In nests on the ground, build domed nests, whereas contrast, a bird incubating in an enclosed nest is 92% of 63 species that build their nests above more likely to be trapped in the nest by a pred- the ground, build open-cup or open-bowl nests ator at the entrance. Antbirds generally, and (Ali and Ripley 1971, 1972). manakins (Pipridae), have open-cup nests usu- Nests placed at the periphery of trees, es- ally located in the lower levels of the tropical pecially when over open spaces, may be less forest (Traylor and Fitzpatrick 1982), where the subject to predation than nests placed more in nests often are sheltered from the sun, rain and the interior of the tree canopy. During a 5-year wind by surrounding vegetation, but where pred- period in northeastern Gabon in equatorial Af- ators abound. rica, Brosset (1974) found 550 nests of 110 spe- North temperate regions have a much higher cies of rainforest birds and followed the fate of proportion of passerine species with open-cup 337 of these nests. Location of the nest was nests versus enclosednests, compared to tropical more effective against predators than was con- regions (Collias and Collias 1964, 1984, Rick- cealment: 70% of nests located in small trees of lefs 1969). Walsberg (1981) used photos taken the undergrowth were destroyed as compared to with a -eye lens and found that the cup nests 50% of those nests built at the tip of projecting of Warbling ( gilvus) in the western twigs, and only 35% of those nests overhanging United States were so placed in a tree as to get water. the sun’s warmth in early morning, and yet be Domed nests placed well up in trees often are shaded in the afternoon when there is a danger suspendedfrom drooping twigs near the periph- that the eggs might die from overheating if long ery of the tree, presumably providing less ac- exposed to the hot sun. Hence, cup nests selec- cessibility to arboreal predators. But such a site EVOLUTION OF PASSERINE NEST BUILDING 265 also will expose the nest more to temperature small passerines (Table 5) than among passer- changes, wind, sun, and rain, than sites toward ines in general, where only about half of 68 fam- the interior of the tree which are more sheltered ilies have speciesbuilding domed nests (Collias from the weather. The more peripheral exposed and Collias 1984). Since the great majority of sites should therefore favor evolution of a roof passerine birds are larger than the 24 smallest to the nest. A roof also would help prevent the passerines (Table 5), this comparison supports eggs from rolling out when the nest is tossed the conclusion that domed nests are more char- about by the wind (Collias and Collias 1984). acteristic of very small passerine birds than of Exposure to strong sun and to rain may be larger passerines. more frequent in tropical latitudes. Among Old Six large families in which the species gen- World (), only about one- erally build open nests, but in which a few spe- fourth of 41 speciesin Europe have domed rath- cies of relatively small birds (body length 5 15 er than open nests, compared with about half of cm) build domed nests, are the Thamnophilidae 70 species in West Africa (Collias and Collias, (Myrmetherula gutturalis; Oniki 1979), Turdidae 1984). (Pogonocichla stellata; Maclean 1985), Musci- In conclusion, each basic nest type has eco- capidae ( livingstonei; Maclean logical advantages and disadvantages, depend- 1985), Meliphagidae (;Frith 1979), ing on the nest site in relation to predators, Thraupidae (; Hilty and Brown 1986), weather, and competitors, all favoring evolution and Emberizidae ( minuta; Hilty and of nest diversity among species. Brown 1986). The problems of predation (Lack 1954), en- Two large families in which many species vironmental stress(Walsberg 1985) and energy build open nests and many others domed nests balance (Walsberg 1980) are greatest for small are the Timaliidae and Tyrannidae. In the Ti- birds such as passerines. According to Wals- maliidae, 64 species of babblers building open berg’s calculations, based on averaging multiple nests had an average body length of 21 cm, estimates for species, the smaller species of whereas 25 species building domed nests aver- birds definitely have higher ratios of daily en- aged only 15 cm long (t,, = 4.81, P < 0.005) ergy expenditure to basal metabolic rate. (Ali and Ripley 1971, 1972). But in the Tyran- In order to exaggerate effects of small body nidae, differences in body length between open size for further insights, I compiled a list of the nestersand domed nestersoften are slight (Hilty smallest passerine birds of the world together and Brown 1986). Many tiny New World - with the general, basic type of nest built by each catchers and antbirds, as well as some very specieswhen this information was available. Ta- small birds from other families, build open nests ble 5 lists 24 speciesof tiny birds (< 9 g) from (Table 5), indicating that other factors besides six continents and three major islands. These body size help determine type of nest built. speciesrepresent 23 different genera and 16 dif- However, in general, very small body size is ferent families. Fifteen (63%) of these 24 spe- most often associatedwith building a roof over cies build domed nests (not in holes), seven the nest. (29%) build open cup nests, and two (8%) spe- The Eared Pygmy-Tyrant (Myiornis auricu- cies nest in holes in trees or in the ground. laris: Tyrannidae) is one of the smallest (7 cm, Overhead vegetation may substitutefor a con- 5.3 g) passerine birds of the world. Steven L. structed roof. The (Regulus regulus), Hilty found a nest of this species in northeast the tiniest bird of Europe, always places its deep Argentina (Misiones Province), and I photo- cup nest under a dense leafy branch (Thaler-Kot- graphed it in situ to illustrate the domed nest tek 1988). The White-flanked Antwren (Myr- with side entrance (Fig. 4) of a tiny bird. This metherula axillaris) of tropical America always pensile nest was built of plant fibers, grassstems has a large overhanging or leaves over its and dry bamboo leaves, and was about 2 m up nest which is a deep cup fastened by its rim to in a small tree having many long spines. a twig fork 0.2-4 m up (Hilty and Brown 1986). The question arises that if a domed nest is so Very small birds often seem to have a need for valuable to very small birds, why is it that, with some sort of roof over their nests. very rare exceptions like the sylphs Aglaiocer- Domed nests are more common (found in eus (Hilty and Brown 1986), the tiny humming- about two-thirds of 16 different families) in very birds (Trochilidae) build a cup nest? At least part 266 NICHOLAS E. COLLIAS

TABLE 5. Basic nest types built by the smallest birds (with adequateinformation on nest) on the different continentsand on three major islands. Nest type: H = hole nest; D = domed nest; 0 = open-cup nest.

Length cm, Location and species (weight g) Nest type References* Acanthisitta chloris 8 (6-7.5) H 1, 17 Grey igata 11 (6.4) D 1, 11 Australia Smicrornis brevirostris 8-9 (5.1) D 2, 3 Rufous-crownedEmu-Wren Stipiturus rujceps 14, tail 8 (5.1) D 2, 17 New Guinea Elfin adolphinae 9 (7.4) D 4, 17 Green-backedWarbler Gerygone chloronotu 8 (6.3) D 4, 17 India, Nepal, SoutheastAsia Small minima 8 (4-6) D 5 Tickell’s Dicueum erythrorhynchus 8 (6.3) D 5 Pallas Phylloscopus proregulus 9 (4.5-6.2) D 6 Pygmy Blue Flycatcher Muscicapellu hodgsoni 8 0 18 Africa Grey caroli 8-9 (6.2) D 7 melanotus 9-10 (7.9) D 7 Yellow-bellied Eremomelu icteropygialis 10-l 1 (8) 0 7 Sunbird- coruscans 10-l 1 D 8 Neomixus tenella 10 (6.4) D 8, 17 Europe Goldcrest Regulus regulus 9 (5.4-5.8) 0 9, 10 Long-tailed Tit caudatus 14, tail 9 (8) D 10 Black-tailed GnatcatcherPolioptila melunura 11 (5) 0 11, 12 Bushtit Psaltriparus minimus 10 (5.5) D 11, 13 Lucy’s Warbler luciae 10 (6.6) H 11, 17 South America Short-tailed Pygmy-Tyrant Myiornis ecaudatus 6.5 (4.9) D 14, 15 cinerea 10 (8) 0 16 White-flanked Antwren Myrmotherula axillaris 9 (8.5) 0 14, 16 Ruddy-breastedSeedeater Sporophila minuta 9 (8) 0 14, 16

* I (Gray 1969, Falla et al. 1978). 2 (Frith 1979, Pizzey 1980). 3 (Recher and Major 1994). 4 (Coates 1990). 5 (Ali and Ripley 1974). 6 (Ali and Ripley 1973). 7 (Maclean 1985). 8 (Langrand 1990). 9 (Thaler-Kotteck 1988). IO (Cramp 1993). II (Hamson 1979, Peterson 1990), 12 (Walakrg 1990). I3 (Chaplin 1982). 14 (Hilty and Brown 1986). 15 (Sick 1993), I6 (Stiles and Skutch 1989), 17 (Dunnmg 1993). I8 (Ali and Ripley 1972). of the answer seems to be that hummingbirds nest with silk, enabling the bird to fasten frequently have a sheltering leaf or branch over its nest more effectively to diverse sites, to use the nest, and in addition, hummingbirds may finer and more varied nest materials, and to give conserve energy by nocturnal torpor (Calder a firmer shape to the nest (Collias and Collias 1974), whereas similar-sized , like other 1984). not only is widely available passerine birds which have been studied, do not in nature, but also has great strength and elas- undergo nocturnal torpor (Prinzinger et al. ticity, with a breaking point that can be 100 1992). In this respect, nocturnal torpor substi- times greater than that of high tensile steel (Gos- tutes for the energy-conserving function of a line et al. 1986). A great many tiny passerine roof. Correlated with their small body size, the birds use silk in their nests, including the great Trochilidae also have many (330) species. majority of the species in Table 5. In contrast, One important consequence of small body larger birds often make their nests of twigs (Col- size in passerine birds is the ability to bind the lias and Collias 1984), materials not so easily EVOLUTION OF PASSERINE NEST BUILDING 267

relationship of nest-building behavior and diver- sity to the successof passerine birds. (1) What are the basic nest types among pas- serines? Hole, open (not in holes) and domed (constructed roof) nests are the basic nest types among passerinebirds (Table 1). Open nests are the most frequent type among families of non- passerines and passerines alike, but hole nests and especially domed nestsoccur more frequent- ly among passerines,particularly in very small passerines,than among non-passerines. (2) When did the basic nest types originate in evolution? The basic nest types arose very early in passerine evolution. Hole, open, and domed nests occur among the nine passerine families considered to be most primitive and nearest the ancestral type (Table 2). This was the primary adaptive radiation. (3) What were the subsequent adaptive spe- cializations of basic nest types in the evolution of the largest, most successful families of sub- oscine birds? This was the secondary adaptive radiation. This was illustrated by indicating the diversity of nests based on hole, open, and domed nests in the Tyrannidae, of open-cup nests in Thamnophilidae, and especially by the great diversity of enclosed nests in the Furnari- FIGURE 4. Nest of Eared Pygmy-Tyrant. idae. Nest form and structure often help char- acterize the genus in birds. (4) What conditions led to the origin in evo- bound with silk as are the iiner materials used lution of the basic nest types-hole, open, and by small birds. domed nests-among passerine birds? Hole Very small passerine birds (Table 5) nest on nests provide a relatively stable and protected every continent and in most habitats on land, environment, but expose small birds to intense from cool southern beech forests in New Zea- competition for nest holes. This problem was land (Rifleman) to northern forests in partly solved by construction of open or domed Scandinavia (Goldcrest), and from dry nests in sites of the birds’ own choosing. Open washes in Arizona (Lucy’s Warbler) to lowland nests are generally the most adaptable, but rainforest in the (Short-tailed evolve into domed (roofed) nests, especially in Pygmy-Tyrant). This strengthens the general small passerines,by two main routes: either on conclusion that small body size is a primary ad- the ground where a roof gives added protection aptation that has enabled passerine birds to in- from predators, or at the periphery of trees, vade and to nest in virtually every terrestrial where a pensile nest is less accessible to pred- habitat in the world, except the Antarctic. ators but with greater exposure to sun, wind and weather. The precise type of nest actually CONCLUSIONS evolved in a given taxonomic group depends on The great diversity of nests built by birds of the a balance of factors involving the history of the order Passeriformeshelps explain their success group, the environment, the nest site, body size, as indicated by their enormous number of spe- behavior, and complex habitat and community cies and individuals, and their occupation of relations. most terrestrial habitats over the world. We may The most general conclusion of this review is now answer the four questions which were that adaptable and varied nest-building behavior, posed in the introduction to this review of the combined with small body size and powers of 268 NICHOLAS E. COLLIAS flight, probably played an important role in the BROSSET,A. 1974 La nidification des oiseauxen for& great adaptive radiation and expansion of pas- Gabonaise:architecture, situation des nids et pre- dation. La Terre et la Vie. Revue d’Ecologie Ap- serine birds during the late Cenozoic period, co- pliqute 28579-610. incident with an increase in terrestrial environ- CALDER,W. A., III. 1974. Consequencesof body size mental diversification over the globe and a for avian energetics.Publ. Nuttall Omithol. Club greatly enhanced food supply. No. 15:86-151. CERNY,V. 1973. Parasite-hostrelationships in feather mites. Proc. Int. Congr. Acarology 3:761-764. ACKNOWLEDGMENTS CHANDLER,A. C. 1916. A study of the structureof I thank the Victor Emanuel 1989 tour group of Argen- feathers with reference to their taxonomic signif- tina, especially the leaders, Steven L. Hilty and Mau- icance. Univ. Calif. Publ. Zool. 13:243-446. rice Rumboll, for help in locating nests, including the CHAPIN,J. I? 1953. The birds of the Belgian Congo. nest of Asthenes anthoides. Maurice Rumboll, former- Part 3. Bull. Am. Mus. Nat. Hist. 75A:l-821. ly chief field naturalist of the Argentine Museum of CHAPLIN.S. B. 1982. Energetic significance of hud- Natural History, was especially helpful in showing us dling behavior in Cornion Bus&tits(Psaltriparus various furnariid nestsof different species.I am grate- minimus). 99:429-430. ful to Richard ffrench and Gustav0 Rodriguez for COATES,B. J. 1990. The birds of PapuaNew Guinea. showing us nests of Phacellodomus rujifrons in Ven- Vol. 2. Passerines. Dow Publications, Alderly, ezuela. I thank the caretakersof the Museum of Nat- Queensland,Australia. ural History of Los Angeles County, and the Museum COLLIAS,N. E. 1964. The evolution of nests and nest- of VertebrateZoology, University of California, Berke- building in birds. Am. Zool. 4:175-190. ley, for access to their collection of Furnariidae. A COLLIAS,N. E. 1986. Engineering aspects of nest grant from the ResearchCommittee of the UCLA Ac- building by birds. Endeavour 10:9-16. ademic Senate helped meet costs of preparing the COLLIAS,N. E. 1991. Nests, p. 224-230. In M. Brooke manuscriot.Elsie Collias. Steven Hiltv, Thomas How- and T. Birkhead [eds.], The Cambridge encyclo- ell, Maurice Rumboll, Betsy Trent Thbmas, and David pedia of . Cambridge Univ. Press, Winkler kindly read earlier versionsof the manuscript Cambridge. and made useful comments. For helpful discussionI COLLIAS,N. E., AND E. C. COLLIAS.1964. Evolution thank E. C. Collias, A. Fedducia, J. W. Fitzpatrick, T of nest-building in the weaverbirds (). R. Howell, W. D. Koenig, W. E. Lanyon, Roxie C. Univ. California Press, Los Angeles. Laybourne, M. L. Morton, S. L. Olson, R. 0. Prum, COLLIAS,N. E., AND E. C. COLLIAS.1984. Nest build- R. Prinzinger, C. G. Sibley, R. J. Raikow, D. Rimlin- ing and bird behavior. Princeton Univ. Press, ger, C. van Riper III, and G. E. Walsberg. I thank Jef- Princeton, NJ. frey A. Gornbein of the UCLA BiomathematicsDe- CRAMP,S. [ED.]. 1977-1994. Handbook of the birds partment for help with the statistics. of Europe, the Middle East and North Africa: the birds of the Western Palearctic. 9 ~01s. 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