The Condor 88:421-439 0 The Cooper Ornithological Society 1986

DETERMINANTS OF GUILD STRUCTURE IN FOREST COMMUNITIES: AN INTERCONTINENTAL COMPARISON’

RICHARD T. HOLMES Department of BiologicalSciences, Dartmouth College,Hanover, NH 03755

HARRY F. RECHER Department of VertebrateEcology, Australian Museum, 6-8 CollegeStreet, Sydney,N.S. W. 2000,

Abstract. We examined the patterns of food resourceutilization (guild structure)of 4 1 species of that breed in eucalypt forestsand woodlands in south temperate Australia, and compared them to the results of a similar study in a north temperate, broad-leaved forest in North America (Holmes et al. 1979). Both studies used the same field methods and analytical techniques. The Australian community was more complex as inferred from the greater number of guilds (9 vs. 4) and from the results of principal components and factor analyses of the foraging data. These multivariate methods showed that guilds at the Australian site were separatedfirst by differences in foraging height and bird weight, and second by foraging methods and food substrates.Use of specific foraging substrates(e.g., exfoliating bark) and food resources(e.g., nectar and other car- bohydrates)were important at finer scalesof separation. The results support the hypothesisthat vegetationstructure and food availability, which vary with speciesand vertical strata,produce particular setsof foragingopportunities for birds. These in turn influence which speciescan obtain food successfully,and thus can be consideredprimary determinants of guild structure.This com- parison of food utilization patterns of birds in contrastinghabitats provides insight into the factors determining bird community organization. Key words: Australianforest birds;bird communityecology; birdforaging; community structure: foliage structure;guild structure;resource availability: resourcepartitioning.

INTRODUCTION (1979) proposed that bird speciescomposition The major goals of avian community ecology in forest habitats depends largely on the for- are to identify recurrent patterns of species aging opportunities afforded by the environ- composition, guild structure, diversity, and ment at any particular site. They suggestedthat other parameters among co-occurring species these were determined primarily by the phys- and to understandthe factors promoting those ical structure of the vegetation, the kinds and patterns (Wiens and Rotenberry 1980). Guild distributions of foraging substrates, and the structure can be defined as the patterns of re- availability of food resources, each of which source use among co-occurring species, with varies among plant species.Additional studies emphasison the similarities and differencesin have shown that insectivorous birds often for- how those speciesexploit resources.For birds age preferentially on certain tree species in terrestrial habitats, food is usually consid- (Franzreb 1978, Holmes and Robinson 198 1, ered to be the important resource, and mea- Airola and Barrett 1985), probably because surementsof foraging behavior are often used they differ in their abilities to sight and capture to indicate how, where, and which food re- prey on with different physical attri- sourcesare obtained. butes (Robinson and Holmes 1982, 1984) and Although bird species have often been as- because of different prey availabilities and signedto foraging guilds on the basisof a gen- abundances (Holmes and Robinson 198 1, eral knowledge of their feeding behavior (Eck- R. T. Holmes and J. C. Schultz, unpubl. data). hardt 1979, Alatalo and Alatalo 1979, Airola These findingslead to the hypothesisthat vege- and Barrett 1985) few studies have identified tation structure coupled with food resource guild structures objectively or have assessed availability and abundance,provide particular the relative importance of the factors that de- combinations of foraging opportunities for fine guilds(e.g., Cody 1974, Holmes et al. 1979, birds that in turn determine which bird species Landres and MacMahon 1980, 1983, Sabo can forage successfullyand survive there. 1980, Sabo and Holmes 1983). The latter stud- The purpose of this paper is to examine the ies show that guild structure varies from site generality of this hypothesisby comparing the to site and is correlated with particular features foragingguild structureof birds in a south tem- of the habitat and resourcebase. Holmes et al. perate, broad-leaved forest in southeastern Australia with that reported by Holmes et al. (1979) for birds in a north temperate broad- ’ ’ Received4 November 1985. Final acceptance24 March leaved forest. The avifaunas at these two sites 1986. have independent evolutionary histories (Sib- W71 428 RICHARD T. HOLMES AND HARRY F. RECHER ley and Ahlquist 1985) and occupy habitats the samethree eucalypt specieson well drained that are broadly similar in structure but which soils, and by swamp gum (E. ovata) where differ in floristics and in some food resources drainagewas impeded. Trees were more widely available to birds. Such a comparison of birds scattered and the canopy slightly more open in contrasting habitats helps to identify the than in the moist forest. Canopy height aver- effects of specific food and habitat character- aged 16 to 20 m. The understory consisted istics on bird foraging, and thus on bird com- entirely of small eucalypts,and the layer munity structure (seealso Cody 1975, Pearson was more open, due to occasional grazing of 1977, Stiles 1978, Landres and MacMahon domestic stock, and some selective logging of 1983, Sabo and Holmes 1983). pole-size trees. The dry forest graded into To facilitate the comparison, we used the woodland dominated by snow gum (E. pau- same field methods and analytical procedures ciflora) and black sally (E. stellulata), which as Holmes et al. (1979). The latter include were shorter (8 to 10 m) than trees in the forest. multivariate statistical techniques that reduce In this woodland, the ground was sparselycov- a large number of correlated variables to a ered with litter, patches of grass (Poa spp.), smaller number of identifiable factors that in- bracken, and sedge.Both dry forest and wood- dicate which variables are most important in land showedevidence of pastburning, but none segregating species and guilds (Cooley and within several years prior to our study. Lohnes 197 1). Note that we use guild in the The climate at Bondi Forest is cool temper- sense of Root (1967) to refer to species ex- ate, with mean monthly temperatures of 18°C ploiting a resourcein similar ways and that we in January and of - 1°C in July (Recher et al. limit our analysesto the avian component of 1983). During October 1980 to January 1981 these communities, acknowledging that other when this study was conducted, night temper- taxa in a more inclusive biological community atures were 5 to 10°C mornings were often may also use some of the same resources(see foggy, and mid-day temperatures climbed to Jaksic 198 1). 20 to 25°C. Rainfall is variable but occurs throughout the year. From 1970 to 1982, it STUDY AREA averaged 1,000 mm per year at Bondi Forest, This study was conducted on the Southern Ta- but in 1980, which was the beginning of a blelands of New South Wales (N.S.W.) and drought, the annual total was only 650 mm Victoria in southeasternAustralia. The three (Forestry Commission, N.S.W., weather rec- 1O-ha study areas were located approximately ords; H. F. Recher, unpubl. data). These study 40 km southeastof Bombala, N.S.W. (36”54’S, areasand their characteristicsare describedin 149”14’E, elevation = 800 to 8.50 m) adjacent greater detail by Recher et al. (1983, 1985) and to Bondi State Forest. Recher and Holmes (1985). The study areas consisted of forest-wood- land ecotone grading from a moist, tall open- METHODS forest through drier, open-forest to woodland at the edge of grazed pastures. The dominant BIRD FORAGING PATTERNS trees in the moist forest were narrow-leaved We quantified foraging behavior of birds at peppermint (Eucalyptus radiata), ribbon gum Bondi Forest between 15 October 1980 and (E. viminalis), and mountain gum (E. dalrym- 15 January 198 1, which was the breeding sea- pleana). Brown barrel (E. fastigata) and mon- son for all species(Recher and Holmes 1985). key gum (E. cypellocarpa) occurred infre- Foraging data were gathered throughout the quently. Canopy height averaged 22 m, with study period, primarily in the morning hours a few trees emergingto 40 m. Young eucalypts, but also at other times of day. Each time a bird with scattered blackwood (Acacia melanoxy- under obervation took or attempted to capture lon) and silver wattle (A. dealbata), formed a a food item, we recorded the foraging method, subcanopyto 13 m in height. The shrub layer the substrate from which the food was taken extended from 1 to 4 m, and was diverse and or towards which the attack was directed, the often dense. It contained mostly Gippsland height above ground (to the nearest m), and, (Teleopea oreades), (Lomatia whenever possible,the type of food taken. An ilicijblia), blackthorn (Bursaria spinosa), and individual bird was followed until a maximum wattles (Acacia spp.). Ground cover consisted of five successiveforaging attempts was re- of ferns (mostly bracken, Pteridium), a sedge corded or the bird was lost from sight. This (Lomandra longijblia), occasional forbs, and procedure increased the chance that the less considerable fallen wood, strips of bark, and conspicuousand/or rarer foraging actionswere leaf litter. There was no evidence of loggingor recorded, and reduced the problem of serial recent burning. dependency (Morrison 1984). Data were ob- The areas of drier forest were dominated by tained from at least 20 to 30 individuals for BIRD GUILD STRUCTURE 429 the more common speciesto at least 6 to 8 for aging charactersfor the multivariate analyses. the lesscommon ones (Table 1). The individ- These consisted of 15 foraging method-sub- uals observed were chosen randomly as we strate combinations (see Table 2 and Appen- moved through the study areas. Some indi- dix) and the 7 vegetation categories listed viduals were undoubtedly observed more than above. We also usedmean foraging height, one once during the study, but never on the same standard deviation of foraging height (to rep- day and rarely in the same week. Sample sizes resent the species’ use of vertical strata), and represent the cumulative number of foraging the species’average body weight (Table 1). The attempts observed for each species(see Table latter was included as an index to bird size; it 1). also servesas an approximate indicator of prey Foraging methods were categorized as fol- size, at least for insectivorous species(cf. Hes- lows: (1) glean-a stationary food item (e.g., penheide 1975). These 25 variables were sim- insect, fruit, nectar) is picked from its substrate ilar to the 27 charactersused by Holmes et al. by a standing or hopping bird; (2) probe or (1979) except that for the present study: (1) prise-like glean only the bird’s beak pene- several unique foraging method-substrate cat- trates or lifts the substrateto locate concealed egorieswere recognized(e.g., glean flower, glean food; (3) hover-a bird takes flight, hovers in loose bark); (2) tree specieswere grouped by a stationary position, sometimes only mo- physiognomic or life-form categories (al- mentarily, near a substrate,and picks the food though these were generally taxonomically-af- item from the substrate’s surface; (4) snatch- filiated groupings);and (3) foragingin the prox- like hover but the flying bird does not hover; imal and distal portions of trees was not instead it plucks the food from the substrate distinguished. as it flies past; (5) pounce-a bird flies from a perch and grabs the food item as it lands on MULTIVARIATE ANALYSES the substrate (usually the ground); and (6) For the multivariate analyses,we followed the hawk- a bird salliesinto the air to catch flying proceduresdescribed by Holmes et al. (1979). prey. This last category is equivalent to “sally” In this case, the data matrix consisted of 41 or “flycatch” as usedby Fitzpatrick (1980) and bird species(rows) by 25 foraging characters others. (columns). The first 22 characters, represent- Substratesfrom which food items were tak- ing utilization frequencies of foraging cate- en were classifiedas: (1) ground, including de- gories, were log-transformed to reduce skew- bris, litter, and grass;(2) trunks- the main axes ness. The last three columns involving mean of trees; (3) branches- smaller secondary axes and SD of foraging height and body weight of trees, > 1 cm in diameter; (4) twigs-small were not transformed. All 25 columns were branches < 1 cm in diameter to which leaves standardizedto bring the means to 0 and vari- were attached; (5) leaves, including leaf blades ances to 1.0, with the result that each mea- and petioles; (6) loose bark-mainly strips or surement was expressedin standard deviation coils of peeling or exfoliating bark most com- units from its column mean. The effect of this mon on upper trunks and branches of certain standardization is to weight all categories speciesof Eucalyptus, but also caughtas debris equally. in the foliage of understory plants; (7) flowers; The 25 foraging character x 41 bird species (8) Eucalyptuscapsules (seeds); and (9) air. matrix was used to calculate Euclidean dis- Plant specieson the study plots were catego- tancesbetween all 4 1 speciesin the hyperspace rized as follows (note eucalypts were grouped defined by the 25 foraging characters(Q-tech- by major physiognomic types): (1) rough- nique of Sneath and Sokal1973). This distance barked eucalypts (E. radiata and E. fastigata) matrix was subjectedto a hierarchical cluster- with rough, corrugated, dark-colored, non-de- ing analysis(maximum method, Johnson 1967) ciduous bark; (2) forest gums (E. dalrym- to produce a dendrogram showingforaging re- pleana,E. ovata,E. viminalis)-large,tall for- lationshipsamong bird species.Principal com- est trees with smooth, light-colored bark that ponents were obtained by multiplying eigen often peelsin long stripsor coils; (3) woodland vectors by the transposed 41 x 25 matrix gums (E. pauciflora,E. stellulata),similar to (Harman 1967). Finally, a varimax rotated forest gums but of smaller size and shorter factor analysis was performed on the 41 x 25 stature; (4) small trees and shrubsof the matrix (R-technique, Sneath and Sokal 1973). Acacia;(5) Gippsland waratah, a shrubbearing Eigen roots > 1.0 were used to calculate an nectar-rich flowers during the period of this orthogonally-rotated factor pattern, following study; (6) other , mostly Lomatia and the procedures of Cooley and Lohnes (197 1). Bursaria;and (7) ground vegetation, mostly The analyseswere run on the Dartmouth Time monocots and ferns. Sharing System, using programs developed by From thesecategories, we recognized 22 for- McGee (1978). 430 RICHARD T. HOLMES AND HARRY F. RECHER

TABLE 1. Characteristicsof the 4 1 common bird speciesbreeding in the eucalypt forestsand woodlands near Bondi State Forest, N.S.W.

Minimum Body weightb numberof Famdy and species Code k) individuals Cacatuidae Gang-gangCockatoo Callocephalonfimbriatum GG 219.0 13.1 * 5.3 8 280 Platycercidae Eastern Rosella Platycercus elegans ER 116.3 10.5 2 5.2 30 1,309 Cuclidae Fan-tailed Cuckoo Cuculuspyrrhophanus FTC 46.3 0.5 ? 1.8 12 100 Menuridae Superb Menura novaehollandiae LB 746.0 0.0 & 0.0 8 62 Campephagidae Black-faced Cuckoo-shrike Coracina novaehollandiae BFC 109.8 11.4 +- 6.0 12 75 Muscicapidae Ground Thrush Zoothera dauma GT 106.2 1.2 * 3.0 10 225 Rose Robin Petroica rosea RR a.7 3.9 & 4.2 10 195 Flame Robin Petroica pheonicea FR 13.3 3.3 * 3.5 30 830 Scarlet Robin Petroica multicolor SR 13.0 1.1 2 2.3 8 465 Eastern Yellow Robin Eopsaltria australis YR 20.0 1.0 ? 2.4 40 408 Eastern Shrike-tit Falcunculus frontatus EST 28.6 11.2 ? 6.3 12 518 Rufous Whistler Pachycephala rujiventris RW 25.8 8.7 ? 5.6 45 983 Golden Whistler Pachycephala pectoralis GW 25.3 5.1 * 4.9 20 551 Grey Shrike-thrush Colluricincla harmonica GST 75.6 4.2 -t 4.2 8 258 Black-faced Flycatcher Monarcha melanopsis BF 23.6 7.0 ? 6.5 8 283 Satin Flycatcher Myiagra cyanoleuca SF 17.5 10.7 * 4.4 22 429 Grey Fantail Rhipidura fuliginosa GFT 9.3 7.3 ? 6.7 80 2,354 Rufous Fantail Rhipidura rufifrons RFI 10.4 1.4 + 1.6 15 303 Orthonychidae Eastern Whipbird Psophodes olivaceus WB 62.2 1.1 ? 1.6 10 133 Maluridae Superb Blue Wren Malurus cyaneus SBW 9.7 0.2 f 0.8 25 803 Acanthizidae White-browed Scmbwren frontalis WBS 12.8 0.3 f 0.8 40 711 Brown Thombill pusilla BT 6.9 2.5 f 2.8 50 1,832 Buff-mmped Thombill Acanthiza reguloides BRT 7.5 1.5 + 2.6 30 559 Striated Thombill Acanthiza lineata ST 7.1 10.3 & 6.4 100 1,331 Yellow-mmped Thombill Acanthiza chrysorrhoa YRT 8.8 0.3 & 1.4 12 378 BIRD GUILD STRUCTURE 431

TABLE 1. Continued.

Minimum Foraging Body weighP Forad;g_h;+&t (m) number of maneuver Family and spec~ev Code (g) -+ individuals sample sized

Neosittidae Orange-wingedSittella Daphoenosittachrysoptera ows 11.9 8.8 k 2.8 18 454 Climacteridae Red-browed Treecreeper Climacteriserythrops RBT 23.3 5.9 t 4.4 16 1,238 White-throated Treecreeper Climacterisleucophaea WTT 21.8 6.1 + 4.2 25 1,224 Meliphagidae Anthochaeracorunculata RWB 99.2 3.1 k 4.2 18 254 Yellow-faced Meliphaga chtysops YFH 17.1 7.0 f 4.8 35 909 White-eared Honeyeater Meliphaga leucotis WEH 24.5 6.8 + 4.6 15 614 Brown-headed Honeyeater Melithreptus brevirostris BHH 14.6 16.7 k 5.0 20 235 White-naped Honeyeater Melithreptus lunatus WNH 14.7 11.9 t 10.3 100 2,805 Phylidonyrispyrrhoptera CHE 16.4 2.7 + 0.6 10 177 Eastern Spinebill Acanthorhynchustenuirostris ESB 10.9 2.2 + 0.8 10 157 Pardalotidae Spotted Pardalotuspunctatus SP 8.3 9.9 + 5.4 15 317 Striated Pardalote Pardalotusstriatus STP 11.9 13.0 ? 5.0 35 810 Zosteropidae Silvereye Zosteropslateralis SE 10.4 7.9 + 6.7 25 530 Corcoracidae White-winged Chough Corcorax melanorhamphus wwc 684.0 0.0 f 0.0 10 250 Artamidae Dusky Woodswallow Artamus cyanopterus DWS 35.7 4.6 ? 2.8 10 145 Cracticidae Australian Magpie Gymnorhina tibicen AM 314.0 0.0 + 0.3 18 622

a Nomenclature follows Condon (1975) and Schodde (1975). B Mean body weights from Recher et al. 1985 and H. F. Recher, unpuhl. data cMinimum number of individuals residing in the study areas, based on average numbers seen per four 4.hour censuses (Recher et al. I985 and H. F. Recher, unpuhl. data). d Sample sizes used in multivariate analyses.

RESULTS birds breeding in this eucalypt woodland-for- At Bondi Forest, there were 41 common est habitat. breeding bird speciesfor which we were able Data used in the multivariate analyses are to obtain relatively large samples of foraging given in Table 1 (mean body weights, mean behavior (Table 1). These ranged in weight foraging heights, and standard deviations of from the 6- to 8-g thornbills to the 746-g lyre- foraging heights) and in the Appendix (the 22 bird. We were not able to obtain data on rap- categories of foraging method-substrate and tors, nocturnally-active birds (e.g., Tawny plant use). The correlation and Euclidean dis- Frogmouth, Podurgusstrigoides; Owlet Night- tance matrices from the multivariate analyses jar, Aegothelescristatus) or several rare species are available from the authors upon request. (see Recher and Holmes 1985) which were Descriptions of the foraging behavior of these difficult to observe. Our analysesare therefore bird speciesare given by Recher et al. (1985) of the common, diurnally active, non-raptorial and Holmes and Recher (1986).

BIRD GUILD STRUCTURE 433

GUILD STRUCTURE: CLUSTER ANALYSIS OF EUCLIDEAN DISTANCE EUCLIDEAN DISTANCES I, 0 9 y I p 5 4 3 2 I 0 CrescentHoneyeater The relationships among the 41 bird species, EosternSplneblll based on the 25 foraging characters,are sum- Red Wottleblrd EasternWhIpbIrd marized in the cluster diagram in Figure 1. The SuperbBlue Wren speciesare separatedinto a number of distinct White- browedScrubwren SIlVereye groupswhose members exploit food resources BrownThornbd in similar ways, and can thereby be considered SpottedPordolote Strmted Pordalole guilds (cf. Root 1967). We define guilds op- Stmted Thornblll erationally as those groups of speciesthat are Oronqe- wmgedSlttello separatedfrom one another by Euclidean dis- Red- browedTreecreeper White-throated Treecreeper tances greater than the mean distance (Z = Eastern Shrlke-IIt 6.9 1, in this case) between all species pairs While-eared Honeyeater Brown-headed Haneyeater (Holmes et al. 1979). Using this arbitrary cri- Whde-naped Honeyeater terion, we recognize nine guilds among the 4 1 Yellow-faced Honeyeater bird speciesat Bondi (Fig. 1). Starting from the top of Figure 1, and basing interpretations on the Appendix (see also Block- faced Flycatcher Recher et al. 1985), we characterize the guilds Golden Whlsller as follows: Guild I contains three Rufous Whistler that fed extensively on nectar obtained from flowers,primarily of Gippsland waratah. Guild II consistsof three speciesthat predominately gleaned prey from ground litter, debris, and low vegetation. The five species in guild III were those that foraged by gleaning prey from I Im , Eastern Rosella foliage and associatedtwigs and small branch- I Gong-gang Cockatoo es. Within this guild, the Silvereye and Brown Superb Lyreblrd Ground Thrush Thombill foraged mostly in the shrub layer, Australian Maqple where they took prey from a diverse array of White-wnged Chough plant species.The other three species-the two FIGURE 1. Cluster diagram of Euclidean distancesbe- and the Striated Thombill-for- tween 4 1 speciesofbirds near Bondi State Forest, N.S.W., Australia, based on their similarities and/or differencesin aged exclusively on eucalypt foliage, mainly in foraging. Dashed line representsthe mean Euclidean dis- the subcanopy and canopy. Guild IV is a tax- tance between all combinations of speciespairs at Bondi. onomically diverse group of 11 species, in- The roman numerals refer to the guilds described in the cluding two thombills, four honeyeaters, a sit- text. tella, two treecreepers, a shrike-thrush, and a shrike-tit, all of which foraged by gleaning but prey but are smaller (9 to 10 g) than speciesin differed in their use of substrates.The sittella Guild II and foraged among the ground and and treecreeperswere bark foragers, with the low shrubvegetation. Guild VII consistsof five sittella foraging mainly on dead branches and speciesthat fed by pouncing on ground- and the treecreeperson the trunks of trees (Appen- trunk-dwelling invertebrates, although the dix). The shrike-tit and White-eared Honey- Dusky Woodswallow frequently took aerial in- eater foraged extensively on hangingand loose sects(Appendix). Guild VIII comprisesthe two or exfoliating bark. Loose hanging bark was parrots which fed almost exclusively on the also used by Brown-headed and White-naped seeds of eucalypts that they extracted from Honeyeaters, but they and the Yellow-faced the ripening capsules.Guild IX contains four Honeyeater were primarily foliage gleaners speciesof large ground foragers (> 100 g body (Appendix). The Grey Shrike-thrush was a weight), and is thereby distinguishedfrom the generalistforager. It used a wide range of sub- much smaller ground-foraging bird in Guilds strates including bark and foliage, but it for- II and IV. The relative importance of these aged extensively on the ground and is grouped various differences and characteristicsamong with the two smaller ground-foraging thom- the nine guilds will be considered below. bills. Guild V contains speciesthat primarily caught flying prey (e.g., Grey Fantail, Satin GUILD STRUCTURE: PRINCIPAL COMPONENTS Flycatcher) or snatchedprey from foliage (two ANALYSIS whistlers, Black-faced Flycatcher, and Black- Another approach to identifying guild struc- faced Cuckoo-shrike) in the subcanopy and ture is to examine patterns revealed by prin- canopy. Guild VI consistsof the Rose Robin cipal componentsanalysis (PCA). The first two and Rufous Fantail which also pursued aerial PC axes in the analysis of the Bondi data ac- 434 RICHARD T. HOLMES AND HARRY F. RECHER

counted for 22.7 and 18.0% of the community 2 of the PCA (Fig. 2) that foraging methods variance, respectively, and provide relatively are the secondmajor set of characteristicsthat interpretable divisions among the species(Fig. segregateguilds. 2). Axis 1 segregatesspecies that forage most- Factor III has negative loadings for ‘Acu- ly in subcanopy and canopy layers (positive cia ” “other shrubs,” and “ground vegetation.” values) from those that forage on the ground This separates shrub-foraging insectivorous or in low vegetation (negative values). Axis II species(e.g., , Golden Whis- separatesspecies that hawk, snatch,and pounce tler) from the shrub-foragingnectarivores (e.g., (positive values) from those that glean, and/or Crescent Honeyeater, Eastern Spinebill). Nec- probe, and prise. Thus, differences in use of tar-feeders are further segregatedon Factor IV, forest strata followed by differencesin foraging which has positive loadings for “glean flower” methods are the primary factors segregating and the plant species,“waratah. ” speciesin how they exploit food resourcesin Although factors V and VIII each account this habitat. The speciesin the PCA (Fig. 2) for ~8% of the variance in community pat- are positioned in ways that closely reflect the terns (Table 2), they help to explain smaller guildsdistinguished in the clusteranalyses (Fig. groupingswithin the community. Factor V has 1). The heterogeneity of guild IV, which con- positive loading for “glean loose bark,” “glean tained 11 speciesaccording to the cluster anal- branch,” and “glean trunk,” separatingthe bark ysis (Fig. l), is upheld by the spread of these foragers (e.g., Eastern Shrike-tit, treecreepers) speciesalong the two PC axes (Fig. 2). from other species(see Appendix). Factor VI The third and subsequentPC axes were not has positive loadings for “glean Eucalyptus easily or clearly interpretable, probably be- capsules” and “mean foraging height,” which causeeach accounted for so little (< 11.5%) of segregatesthe two canopy-foraging parrots the community variance (R. T. Holmes and from the rest of the community (Table 1 and H. F. Recher, unpubl. data; see Table 2). Appendix). Factor VII has positive loadings for “snatch leaf,” “snatch branch,” and “hawk” which distinguishesthe active foragers such as DETERMINANTS OF GUILD STRUCTURE: fantails, flycatchers,and whistlers. Factor VIII VARIMAX FACTOR ROTATION has positive loadings for “forest gums” and The Varimax rotated factor analysis deter- “mean foraging height,” and negative for mines more explicitly which variables or groups “glean ground” and “ground vegetation.” This of variableswere important in segregatingthese reinforces the distinction between foraging bird speciesand guilds (Table 2). The first eight higher in the forest, and foragingon the ground, eigen vectors extracted from the correlation or in low vegetation as found with Factor I. matrix had values ~1 .O, and accounted for 8 5% of the community variance (Table 2). Fol- lowing Aspey and Blankenship (1977), we only COMPARISONS AND DISCUSSION list factor loadings in Table 2 that are >0.45, Since it is difficult to compare guild structures becauselower values share ~20% of the vari- without objective or standardized techniques, ance with a particular factor. we focus this discussionon the patterns of bird Factor I has positive loadings for “rough- guild structure at Bondi and in the northern barked eucalypts,” “woodland gums” and hardwoods forests at Hubbard Brook in New “standard deviation of foraging height” and Hampshire (Holmes et al. 1979) which were negative values for “probe ground” and “body studied with the same field methods and an- weight” (Table 2). Thus, birds that foraged on alytical techniques. These two studies also these trees had broad foraging height ranges considered the same range of species,i.e., all and differed from those large (heavy) species of the common, diurnally-active, nonrapto- that probed on the ground. This separation of rial breeding bird speciesoccupying the study birds that forage at many heights above the areas. Although other studies of bird foraging ground from ground foragers confirms the relations in forested habitats have been made, above interpretation of the first PCA axis, i.e., for example, by Cody (1974), Landres and guildsare first segregatedby height. These find- MacMahon (1980,1983), Sabo (1980) Alatalo ings also suggestthat differences in body size (1982), and Airola and Barrett (1985), these may be involved in segregatingspecies. have either used different techniques (Cody, Factor II has positive loadings for “pounce Landres and MacMahon, Sabo) or have con- ground” and “snatch trunk,” and negative sidered only some components of the avian loadings for “hover leaf” and “glean leaf, twig assemblage(Alatalo, Airola and Barrett). The and branch.” This separatesthe speciesthat only studies quantifying bird foraging behav- pounce on their food from those that primarily ior in Australian habitats are those of Crome glean, and supportsthe interpretation of Axis (1978) and Frith (1984) in Queensland rain- BIRD GUILD STRUCTURE 435

t 3.01 4 W GroundForogers- AXIS I -Above-ground Foragers FIGURE 2. Projection of 4 1 bird speciesalong the first two principal component axes, based on foragingdata. Axes I and II accountfor 23% and 18% of total variance, respectively. Encircled speciesgroups are those identified as guilds T TV :_ rl-^ ^1.._.____..,..___ ,F1_ 1, O^^-r-L,_ 1 r______:__ _..-L^I_

forests, Thomas (1980) in a temperate rain- structure, bird speciesrichness, and the his- forest in Tasmania, and Ford et al. (in press) torical factorswhich have influencedall of these in a eucalypt woodland near Armidale in features, the avian guild structures at Bondi northeastern N.S.W. None, however, used Forest and Hubbard Brook are basically sim- multivariate statistical techniques to identify ilar. The guilds at both sitesare separatedinto factors underlying guild structure. foliage-, bark-, and ground-foraginggroups, and The habitats and avifaunas at Bondi Forest these are further subdivided by differences and Hubbard Brook are broadly similar in a among species in their use of foraging sub- number of ways, yet differ in important details. strates and methods, and in body size. The Bondi Forest is characterized by a relatively Australian community, however, is more mild climate, the vegetation is composed of complex as evidenced by (1) the greater num- sclerophyllous,mostly evergreen,broad-leaved ber of species(41 vs. 22) and guilds (9 vs. 4), trees, dominated by 3 to 4 speciesof Eucalyp- (2) the emergencein the factor analysisof more tus, and there are 4 1 common bird speciesthat eigen roots with values > 1 (8 vs 5), (3) more breed in this forest-woodland ecotone. At equitable distribution of variance among the Hubbard Brook, the climate is more strongly different factors (the first two factors combined seasonal,with long, cold, snowy winters and accounted for only 40.8% of the variance in warm, moist summers, the vegetation is dom- the Australian community compared to 60.9% inated by 3 speciesof broad-leaved deciduous for Hubbard Brook), and (4) by the less easily trees, and there are 22 common breeding bird interpreted multivariate axes, especially in the species.The avifaunas at the two sitesare phy- PCA. In the Hubbard Brook analysis, the fac- logenetically distinct (Sibley and Ahlquist tor analysis produced fewer, more heavily 1985). The forest structure at both sites is weighted and more clearly interpretable fac- roughly comparable, with canopy heights av- tors (Holmes et al. 1979). Also, speciesin the eraging 20 to 30 m, although physical char- Australian community are generally more spe- acteristics of the vegetation (e.g., leaf shapes cialized in their foraging, using one or at most and sizes, branching patterns) differ consid- two of the major foraging method-substrate erably (see below). combinations (Appendix). At Hubbard Brook, In spite of these differencesin climate, plant most specieshave broader foraging repertoires 436 RICHARD T. HOLMES AND HARRY F. RECHER

(Holmes et al. 1979, Robinson and Holmes and succeedingfactors in the Hubbard Brook 1982, R. T. Holmes and H. F. Recher, unpubl. analysis. As at Hubbard Brook, plant species data). in the south temperate eucalypt forestsin Aus- Some of these differences, especially the tralia support different food resourcesfor birds number of speciesand guilds, are related to (Ohmart et al. 1983, Recher et al. 1983, Woin- the ecotonal forest and woodland habitat con- arski and Cullen 1984) and have different fo- sidered at Bondi Forest. However, analysesof liage arrangements and substrates on which data from only the moist forest at Bondi For- prey may sit or within in which they may hide est, which is more directly comparable to Hub- (see below). These characteristics,which also bard Brook (26 vs. 22 bird species, similar vary over the vertical profile of a forest, pro- canopy heights, etc.) but for which we had rel- duce particular sets of foraging opportunities atively small sample sizesof bird foraging be- for birds, which, as shown by the resultsof the havior, show the same differencesin complex- multivariate analyses here, are important as ity as enumerated above (R. T. Holmes and segregatorsof guilds. If such foraging opportu- H. F. Recher, unpubl. data). It therefore seems nities are correlated with increased vegeta- that more diverse factors must be influencing tional complexity, this would help to explain the foragingpatterns and guild structureof birds the findings of MacArthur and MacArthur in the Australian forest. Comparisons of the (1961), Recher (1969) and others that bird two communities help to elucidate the factors speciesdiversity is related to vegetational di- underlying these differences and to identify versity, but in this case,the importance of plant’ what aspects of the environment determine speciesand their different physiognomies,and guild structure at each site. associatedfood resourcesis emphasized. Plant The initial separation of guilds in the Aus- speciesand their differing structuresmay also tralian community was related to birds’ dif- be important in the latter regard by providing ferential use of vertical strata, particularly suitable nest sites,especially for cavity nesters ground versus above-ground foraging. The oc- (Recher and Holmes 1985). currence of body size on the first factor can be Several contrasting features of the habitats attributed to the influence of three large species at Bondi Forest and Hubbard Brook illustrate (Superb Lyrebird, White-winged Chough, and how forest structure and available food re- Australian Magpie), which foraged exclusively sourcesinfluence bird foraging and thus guild on the ground, thus accentuatingthe body size- structure. For instance, at Bondi, the canopy low stratum relationship. Since the first factor is relatively open and the foliage is evenly separatingguilds at Hubbard Brook was also spacedwith leaves that are long, narrow, and height-related (Holmes et al. 1979, see also hang vertically. This means that branchesand Sabo and Holmes 1983), forest stratification other perch sites for birds are typically sepa- seemsto be a major factor segregatingspecies, rated from the foliage by relatively long dis- suggestingthat foraging opportunities for birds tances, which in turn requires those species in these forests differ with height. that search foliage to scan for prey over long The second major factor separating guilds distances. This may explain the greater fre- at Bondi Forest was related to differences in quency of speciesat Bondi Forest that hover, foraging methods, especially how birds ob- snatch or hawk their prey and that have cor- tained their food (foraging method) and the respondingly longer prey-attack distances, substratesfrom which prey were taken. This compared to those at Hubbard Brook (Holmes contrastswith Hubbard Brook where foraging and Recher 1986). At the latter site, the foliage zones (tree boles versus more distal foliage) is denser and more clumped along branches, were the major categorieson the second axis. which makes gleaning close to perches more This latter dichotomy may be more distinct in feasible, and perhaps more productive. the north temperate forest becauseof the pres- A second example concerns the effects of ence of bark-burrowing insects and of birds foliage density in the shruband litter layer, and (woodpeckers: Picidae) that excavate these the availability of food resources there. At prey. At the Australian site, such prey were Bondi Forest, the relatively open shrub layer, lacking or at least unavailable in the dense especially in the drier forest and woodland, eucalypt wood (G. Gowing and H. F. Recher, coupled with the presence of low exposed unpubl. data), and no birds at Bondi Forest percheswith views to the ground and the avail- fed by probing or drilling into eucalypt trunks ability of large surface-active prey such as bee- or branches. tles and small lizards (G. Gowing and H. F. Finer divisions of guildsat Bondi Forest were Recher, unpubl. data), provide foraging op- related to the effects of different plant species, portunities for bird species,such as the mus- or physiognomies,and bird foraging methods, cicapid robins and the Fan-tailed Cuckoo, that coinciding with the interpretations of the third pounce on ground-dwelling prey. In the Hub- BIRD GUILD STRUCTURE 437 bard Brook forest, the vegetation in the shrub structure (e.g., foliar arrangements, position- and ground layers is dense, litter is thick, there ing and accessibility of available substrates) are few large prey active on the forest floor, at and the types and availabilities of food re- least during the day, and the pouncing foraging sources strongly influence how birds forage. method is used only rarely (R. T. Holmes and Since foliage structure and resource availabil- S. K. Robinson, unpubl. data). ity change over the vertical profile of forests At Bondi Forest, particular plant species and vary with plant species,they act in con- provide food resources for birds that are not junction with forest stratification to shape the available in the north temperate forest. The kinds of foraging opportunities that can be ex- eucalypts have seeds in large, hard capsules, ploited by birds. These characteristicsin turn which are fed upon almost exclusively by the influence which species can successfullyex- two speciesof parrot. No equivalent resource ploit food there, and therefore can be consid- is available to breedingbirds at Hubbard Brook ered primary determinants of guild structure. and no seed-eatingguild is presentthere during Other processes,such as historical factors that the breeding season.Also, many of the plants determine the available speciespool and com- at Bondi Forest, such as waratah and the eu- petition among speciesfor available resources, calypts, provide nectar resourcesthat are fed will also affect which particular species are upon extensively by birds such as honeyeaters present, the numbers of speciesper guild, and and silvereyes. Furthermore, such nectar pro- more subtle relationshipsamong species(Sabo duction is not synchronous(Recher et al. 1983), and Holmes 1983). resulting in the need for nectar-feeding birds Further comparisons of guild structures of to shift their use of plant species seasonally. birds in both similar and contrasting habitats Plants at Bondi Forest also produce, either di- are needed to clarify the importance of vege- rectly or indirectly, other types of carbohydrate tation structure and food resources in deter- materials, suchas manna (bark exudates),hon- mining bird community structure. Like the eydew (insect secretions)and lerp (sugarycoat- present study, however, the results of such ing of jumping plantlice, Psyllidae:Homop- comparisons are correlational and can only tera), that are used as food by honeyeaters, suggestwhat may be the underlying causal silvereyes, pardalotes, thornbills, and others agents. Thus, more direct investigations de- (Paton 1980, Woinarski 1985, Ford et al., in signed to test how foliage structure and food press). The relative abundance of these also availability affect the foraging success,habitat varies among plant species (Paton 1980, selection,and ideally the survival of individual Woinarski and Cullen 1984). The only similar birds and speciesare also urgently needed. resourceat Hubbard Brook is tree sap utilized by the Yellow-bellied Sapsucker(Sphyrapicus ACKNOWLEDGMENTS varius)and its commensal, the Ruby-throated Hummingbird, (Miller and This research was supported by the National Science Archilochuscolubris Foundation (U.S./Australia Cobperative Science Pro- Nero 1983). cram). the National Parks and Wildlife Service (N.S.W., As a final example, the exfoliating bark of Lus&ia), the Forestry Commission (N.S.W.),‘ Harris- forest and woodland gumsat Bondi Forest pro- Daishowa Pty. Ltd., Dartmouth College, and the Austra- vides specialized foraging opportunities for lian Museum. The Victorian Forestry Service allowed us to work in the forests along Coast Range Road, Victoria. birds. These strips of peeling bark harbor var- G. Gowing, R. Kavanagh, W. Rohan-Jones,J. Shieldsand ious insectsand spiders,which were exploited M. Schulz assistedwith the field work. We thank M. L. specificallyby White-eared and Brown-headed Morrison, N. L. Rodenhouse, G. Pyke, S. K. Robinson, Honeyeaters, Eastern Shrike-tits, and Whip- T. W. Sherry, B. B. Steele, and C. J. Whelan for their critical but helpful comments on the manuscript and Dr. birds. The first three speciessearched for prey T. W. Sherry for his assistancewith the multivariate anal- on this foraging substratehigh in the canopy, yses. while the Whipbird foraged most commonly among piles of fallen bark on the ground. No comparable foraging substrate/resource is LITERATURE CITED available to birds at Hubbard Brook, although AIROLA,D. A., AND R. H. BARRETT.1985. Foragingand Winter Wrens (Troglodytestroglodytes) often habitat relationshipsof insect-gleaningbirds in a Sier- searchedfor food on the bark of fallen branch- ra Nevada mixed-conifer forest. Condor 87:205-216. ALATALO,R. V. 1982. Multidimensional foraging niche es and boles (Holmes et al. 1979), and thus organizationof foliage-gleaningbirds in northern Fin- show some similarity to the Whipbird. land. Omis Stand. i3:56-71. In conclusion, this analysis of foraging guild ALATALO.R. V.. AND R. H. ALATALO. 1979. Resource structure among birds in a eucalypt forest- par&oning’among a flycatcherguild in Finland. Oi- kos 33:46-54. woodland, when contrasted with the results ASPEY,W. P., ANDJ. E. BLANKENSHIP.1977. Spidersand from a similar study in a north temperate for- snailsand statisticaltales: application of multivariate est, supports the hypothesis that vegetation analysesto diverse ethologicaldata, p. 75-120. In B. 438 RICHARD T. HOLMES AND HARRY F. RECHER

A. Hazlett [ed.], Quantitative methods in the study samplingdesign on analysesof avian foragingbehav- of behavior. Academic Press, NY. ior. Condor 86: 146-150. CODY, M. 1974. Competition and the structure of bird OHMART,C. P., L. G. STEWART,AND J. R. THOMAS. 1983. communities. Monogr. Popul. Biol., Princeton Univ., Phytophagousinsect communities in the canopiesof NJ. three Eucalyptus forest types in south-easternAus- CODY,M. 1975. Towards a theory of continental species tralia. Aust. J. Ecol. 8:395-403. diversities: bird distributions over Mediterranean PATON,D. C. 1980. The importance of manna, honey- habitat gradients, p. 214-25 1. In M. L. Cody and J. dew and lerp in the diets of honeyeaters. Emu 80: M. Diamond [eds.], Ecology and evolution of com- 213-226. munities. Belknap Press, Cambridge, MA. PEARSON,D. L. 1977. A pantropical comparison of bird CONDON, H. T. 1975. Checklist of the birds of Australia. community structureon six lowland forest sites.Con- Part I, Non-.Royal Australasian Ornitho- dor 791232-244. logical Union, Melbourne. RECHER,H. F. 1969. Bird speciesdiversity and habitat COOLEY,W. W., AND P. R. LOHNES. 1971. Multivariate diversity in Australia and North America. Am. Nat. data analysis.John Wiley and Sons, NY. 103:75-80. CROME,F.H.J. 1978. Foraging ecologyof an assemblage RECHER,H. F., G. GOWING,R. KAVANAGH,J. SHIELDS, of birds in lowland rainforest in northern Queensland. AND W. ROHAN-JONES.1983. Birds, resourcesand Aust. J. Ecol. 3:195-212. time in a tablelands forest. Proc. Ecol. Sot. Aust. 12: ECKHARDT,R. C. 1979. The adaptive syndromesof two 101-123. guilds of insectivorousbirds in the Colorado Rocky RECHER,H. F., ANDR. T. HOLMES. 1985. Foragingecol- Mountains. Ecol. Monogr. 49: 129-149. ogy and seasonalpatterns of abundance in a forest FITZPATRICK,J. W. 1980. Foragingbehavior ofneotrop- avifauna, p. 79-96. In A. Keast, H. F. Recher, H. A. ical tyrant flycatchers.Condor 82143-57. Ford and D. Saunders[eds.], Birds of eucalypt forests FORD,H. A., S. NOSKE,AND L. BRIDGES.In press. For- and woodlands: ecology, conservation and manage- aging behaviour of birds in eucalypt woodland in ment. Surrey-Beatty, Sydney. northeasternNew South Wales. Emu. RECHER,H. F., R. T. HOLMES,M. SHULTZ,J. SHIELDS,AND FRANZREB,K. E. 1978. Tree species used by birds in R. KAVANAGH. 1985. Foraging patterns of birds in loggedand unloggedmixed coniferousforests. Wilson eucalypt forest and woodland on the tablelands of Bull. 90:221-238. southeasternAustralia. Aust. J. Ecol. 10:399-42 1. FRITH, D. W. 1984. Foraging ecology of birds in an up- ROBINSON,S. K., AND R. T. HOLMES. 1982. Foraging land tropical rainforest in North Queensland. Aust. behavior of forestbirds: the relationshipamong search Wildl. Res. 11:325-347. tactics, diet and habitat structure. Ecology 63: 1918- HARMAN,H. H. 1967. Modem factor analysis.2nd edi- 1931. tion. Univ. of Chicago Press, IL. ROBINSON,S. K., AND R. T. HOLMES. 1984. Effects of HESPENHEIDE,H. A. 1975. Prey characteristicsand pred- plant speciesand foliage structureon the foragingbe- ator niche width, p. 158-180. In M. L. Cody, and J. havior of forest birds. Auk 1011672-684. M. Diamond [eds.], Ecology and evolution of com- ROOT,R. B. 1967. The niche exploitation pattern of the munities. Belknap Press, Cambridge, MA. blue-grey gnatcatcher.Ecol. Monogr. 37:3 17-350. HOLMES,R. T., R. E. BONNEY,JR., AND S. W. PACALA. SABO,S. R. 1980. Niche and habitat relations in subal- 1979. Guild structure of the Hubbard Brook bird pine bird communities of the White Mountains of community:a multivariate approach.Ecology 60: 5 12- New Hampshire. Ecol. Monogr. 50:241-259. 520. SABO, S. R., AND R. T. HOLMES. 1983. Foraging niches HOLMES,R. T.. AND H. F. RECHER. 1986. Searchtactics and the structureof forest bird communities in con- of insectivorous birds foraging in an Australian eu- trasting montane habitats. Condor 85: 12 l-l 38. calvnt forest. Auk 103:515-530. SCHODDE,R. 1975. Interim list of Australian . HoLM&,~R. T., ANDS. K. ROBINSON.198 1. Tree species Royal Australasian Ornithological Union, Mel- preferencesof foraginginsectivorous birds in a north- bourne. em hardwoods forest. Oecologia 48:3 l-35. SIBLEY,C. G., AND J. E. AHLQUIST. 1985. The phylogeny JAKSIC,F. M. 1981. Abuse and misuseof the term “guild” and classificationof the Australo-Papuan passerines. in ecologicalstudies. Oikos 37:397-400. Emu 85:1-14. JOHNSON,S. C. 1967. Hierarchical clustering schemes. SNEATH,P.H.A., AND R. R. SOKAL. 1973. Numerical Psychometrika 32:241-254. . W. H. Freeman and Company, San Fran- LANDRES,P. B., AND J. A. MACMAHON. 1980. Guilds cisco. and community organization: analysis of an oak STILES,E. W. 1978. Avian communities in temperate woodland avifauna in Sonora, Mexico. Auk 97:35 l- and tropical alder forests. Condor 80:276-284. 365. THOMAS,D: G. 1980. The bird community of Tasma- LANDRES.P. B.. AND J. A. MACMAHON. 1983. Com- nian temperate rainforest. Ibis 122:298-306. munity organization of arboreal birds in some oak WIENS,J. A.,AND J. T. ROTENBERRY.1980. Bird com- woodlandsof western North America. Ecol. Monogr. munity structure in cold shrub deserts:competition 53:183-208. or chaos.Proc. XVII Int. Omith. Congr.(Berlinl: 1063- MACARTHUR,R. H., ANDJ. W. MACARTHUR. 1961. On 1070. bird speciesdiversity. Ecology 42:594-598. WOINARSKI,J.C.Z. 1985. Foliage gleaners of the tree- MCGEE. V. 1978. The multivariate nackaee of BASIC tops: the nardalotes. D. 165-175. In A. Keast. H. F. programs. 3rd ed. Amos Tuck School-of Business R&her, I?. A. Ford’and D. Saunders[eds.]. Birds of Administration, Dartmouth College, Hanover, NH. eucalypt forests and woodlands: ecology, conserva- MILLER,R. S., AND R. W. NERO. 1983. Hummingbird- tion and management. Surrey-Beatty, Sydney. sapsuckerassociations in northern climates. Canad. WOINARSKI,J.C.Z., AND J. M. CULLEN. 1984. Distribu- J. Zool. 61:1540-1546. tion of invertebrates on foliage in forests of south- MORRISON,M. L. 1984. Influence of sample size and eastern Australia. Aust. J. Ecol. 9:207-239. BIRD GUILD STRUCTURE 439

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