secondary succession and breeding bird community structure: patterns of resource utilization

Oecologia (Berl) (1982) 55:208-216 Oecologia �9 Springer-Verlag 1982

Secondary Succession and Breeding Bird Community Structure: Patterns of Resource Utilization P.G. May George Mason University, Fairfax, Virginia, USA

Summary. Structure of breeding bird communities was compared among four habitat types representative of stages present in most old-field successions in the eastern deciduous forest formation of North America. The successional catagories, defined by vegetational structure, were designated herbaceous (type A habitats), herb, shrub and sapling (type B), young forest (type C), and older forest (type D). Density of breeding birds was lowest in A habitats, rose sharply in B habitats and reached a maximum in D habitats. Species richness and number of feeding guild showed similar patterns. Mean number of species per guilds was highest in D habitats. Generalist feeding guilds were predominant in type A and B habitats, primarily due to the importance of the graminivore-insectivore guild. Specialist guilds increased in importance with succession due to addition of several insectivorous guilds in later successional stages. Pat- terns of occurrence of individual feeding guilds are analyzed and discussed with respect to changes in vegetational structure. Variance in community structure was generally highest in A habitats and lowest in D habitats; this is discussed in relation to the evolution o f " saturated", coadapted communities.

Introduction

Ecological succession is one of the most firmly entrenched concepts of ecology, yet many of the mechanisms and prop- erties of succession are still quite controversial (McIntosh 1980; Egler 1981). Most of the controversy has centered around the vegetational aspects of succession. Animal eco- logists however, have found successional changes of the plant community to be a useful framework on which to base comparative studies of animal communities. A sub- stantial literature has developed concerning avian community structure in relation to successional stage (Adams 1908; Beedy 1981; Johnston and Odum 1956; Karr 1968, 1971; Kendeigh 1946; Kricher 1973; Odum 1950; Saunders 1936; Shugart and James 1973; Smith and MacMahon 1981; Stiles 1980).

These studies have focused on a variety of aspects of avian community structure, emphasizing changes in species composition, density and species diversity of breeding bird communities. Generalizations that have emerged from this

Offprint requests to." P. May, Department of Zoology, University of Florida, Gainesville, Florida 32611, USA

work include trends toward increasing species diversity and richness with succession (Adams 1908; Johnston and Odum 1956; Karr 1968, 1971; Kricher 1973; Shugart and James 1973). Other studies of avian community structure have implicated changes in the diversity of vegetational structure as a major factor influencing avian diversity (MacArthur 1964; Karr 1968; Willson 1974). The causal relationships between vegetational structure and avian diversity have usually remained obscure, however (Holmes et al. 1979), somewhat limiting the usefulness of this approach.

Aside from more obvious aspects of community structure such as density and diversity, little attention has been given to other equally important aspects of community structure such as the patterns of resource utilization among successional communities. Willson (1974) and Karr (1971) have given some consideration to this aspect of community structure. Ecological and successional theory would predict certain changes in resource utilization patterns accompany- ing succession. Odum (1969) predicted a change in feeding strategies with succession, with generalists predominating in early successional communities and specialists predominating in mature habitats. Niche theory predicts an increase in specialization with increasing stability of environmental conditions (Pianka 1976). Temporal stability (i.e., persistence), of the seral stage tends to increase with succession, thus predicting changes similar to those predicted by Odum (1969). Whittaker and Goodman (1979) predict that in environments in which carrying capacity varies widely (i.e., un- stable environments), opportunism should be favored (their "exploitation adapted" species), whereas in environments with a more stable K (" saturation adapted"), interspecific effects should be important in structuring life history tactics. Presumably, competition among "saturation- adapted" species will result in selection for specialization.

In this study, I reexamined the changes in density and diversity of breeding bird communities inhabiting several successional stages in light of changes in resource utilization. In addition, I used replicates within each successional catagory, allowing examination of a) patterns of variance in community structure as well as b) detection of statistically significant changes in community composition. These two aspects have been lacking in earlier studies of avian communities and succession.

Methods and Materials

The source of the data was 40 breeding bird censuses pub- lished in American Birds (Audubon Field Notes). These

0029-8549/82/0055/0208/$01.80

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censuses are summarized in Table 1 and listed in the Appen- dix. Breeding bird censuses are conducted using the spot- map method (Van Velzen 1972; Robbins 1978), and for the purposes of this study each census was designated a community. I divided the censuses into four successional catagories which were defined by vegetation structure and representative of common phases of old-field successions throughout the eastern U.S. (Johnston and Odum 1956; Bard 1952; Dale and Fullerton 1964; Oosting 1942; Quar- termain 1957). The four categories are herbaceous plots (hereafter type A habitats) defined by presence of a more or less even monolayer of herbaceous vegetation, character- istic of the first few years of succession after disturbance; herb, shrub and sapling plots (type B), composed of a mixture of herbaceous species as well as invading woody plants which have not yet formed a canopy; young forest (type C), defined by development of an essentially closed canopy and average diameter breast height of 25.4 cm (10") or less; older forest (type D), defined by presence of closed canopy and an average DBH of dominant tree species of greater than 30.5 cm (12"). Each successional catagory con- tained 10 censuses.

I compared communities among successional stages for differences in mean density and mean species number. Density was standardized to number of territorial males per 40 ha for the calculations of mean density per successional stage. Species which were assigned a density of less than 0.5 males per census were excluded from the analysis. I assigned each species to a feeding guild based on the classifications of Cody (1974), Willson (1974), behavioral information from the literature and dietary information from Martin et al. (1951). The guilds recognized were frugi- yore, graminivore, raptor, aerial flycatcher (insects caught in continuous flight), sallying flycatcher (insects caught in brief flights from a perch), ground insectivore (diet includes non-insect invertebrates as well), undergrowth insectivore (low foliage gleaner), canopy insectivore (high foliage gleaner), twig and branch insectivore, trunk surface insectivore, graminivore-insectivore, frugivore-insectivore, nectarivore-insectivore and omnivore. I placed a species into a single-item guild (the first 10 listed above) if seeds, animal matter or fleshy fruit made up more than 80% of the spring and summer diet, and in a multiple item guild if seeds, animal matter and/or fruit each constituted more than 20% of the spring and summer diet. The classification of species into feeding guilds is included in the appendix. The mean number of guilds per successional category was compared among categories. In all comparisons among successional categories described above or hereafter, a Kruskal-Wallis one-way analysis of variance was used to determine significant differences.

The density, number of species and relative importance (% of total density) of each guild was calculated for each community. Means of these figures were compared among the four categories. I classified each guild as '~ specialist" (single food type), or "generalist" (multiple food types). Relative importance of generalists and number of generalist and specialist species were calculated for each community. Means of these figures were compared among successional categories.

Results

The census plots are listed in Table 1, along with density (territorial males/40 ha), species number and number of

guilds in each community, as well as area and location of the census plot. Only census plots between 6 and 16 ha were chosen for the analyses so as to minimize any species-area effects (Conner and McCoy 1979; James and Rathbun 1981). Note, however, that although the range of plot areas within each category is similar for the four categories, mean plot size is slightly smaller in later successional categories (x= 10.7 ha in type A plots vs. 7.4 ha in type D plots). As species numbers and densities are greatest in type D habitats, the differences reported here are conser- vatively biased due to the smaller mean area of these plots.

The mean density, species number and guild number, as well as mean number of species/guild and associated variances are presented in Table 2. The trends recognized by most previous authors of increasing density and species number with successional age are evident in these data also, although a slight drop is seen between type B and C habitats. The rise in guild number is quite rapid between type A and B communities, but only two guilds are added once woody invasion is under way. Increase in number of species with successional age can be attributed to two factors; an increase in the number of guilds per community and an increase in number of species/guild (seen only in type D habitats). Notice that relative variance as determined by the coefficient of variation (CV = s.d./2 x 100) is highest for

a l l of these characteristics in type A habitats, and decreases to a minimum in mature (type D) habitats.

The comparisons involving generalist/specialist composition of communities are presented in Table 3. Note that while number of generalist species per community shows no consistent trend, generalists are clearly dominant in the early successional categories and generally decrease with successional age. Interestingly, number of generalist guilds per community is higher in B, C and D habitats than in A habitats, but this is balanced by a decrease in mean number of species per guild, with generalist guilds in C and D habitats tending toward about one species each. Number of specialist guilds and species consistently increase with succession, and in addition the mean number of species per specialist guild also increases to a maximum in D habitats. The importance of non-paserines in the community also shows a consistent increase with successional age.

Again, variance shows rather consistent patterns of change for all comparisons. Regarding specialist composition (number of species, number of guilds and number of species/guild), variance is highest in A habitats and lowest in D habitats, whereas generalist composition generally shows an opposite trend. As the numerical importance of generalists drops drastically between A and D habitats however, the implication is that type D communities are much more uniform in structure and composition than communities inhabiting earlier successional habitats.

The patterns of change evidenced in Tables 2 and 3 are clarified by the analyses of individual guilds presented in Tables 4 and 5, which illustrate changes in importance of generalist and specialist guilds respectively. It is clear from Table 4 that the numerical dominance of generalists in early successional habitats is due to the importance of the graminivore-insectivore guild. This guild, which con- tains mainly icterids and fringillids, is the most important guild in the community in type A and B habitats. Frugi- vore-insectivores show a peak of importance in B habitats, one of the few guilds to show such a pattern. Omnivorous species (defined here as species feeding on seeds, animal

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Table 1. Census plots utilized in analyses

Census name Density" Species # Guild # Area(ha) Location

Type A habitats

Two ungrazed fields 80 7 2 8.1 Ohio Abandoned field 81 4 2 10.5 Ontario Old field 18 a 1 14.5 Kansas Abandoned field 214 8 3 6.1 Maryland Open field a 22 7 2 13.0 New York Recently abandoned pasture 45 3 3 1 2 . 3 Pennsylvania Abandoned turf field 58 4 2 6.3 Maryland Abandoned old field 64 7 3 9.7 Indiana Bluegrass-timothy-clover old pasture 69 6 2 14.2 Illinois Orchard grass-tall fescue meadow 103 5 3 12.1 Illinois

Type B habitats

Avanced old field 88 8 4 8.5 Indiana Overgrown pasture field 140 13 7 6.1 West Virginia Upland field, overgrown 167 9 4 6.1 West Virginia Shrubby field 244 17 8 6.7 Pennsylvania Wet shrubby fields 301 25 10 16.2 Pennsylvania Brushy field bottomland 263 21 7 6.1 West Virginia Upland brushy pasture 255 20 8 8.5 Connecticut Overgrown field 225 17 8 13.0 North Carolina Old field habitat 307 9 5 7.3 New Jersey Abandoned field and pasture 177 15 7 9.8 Indiana

Type C habitats

Young Oak forest 74 7 3 6.1 West Virginia Young mixed hardwoods-pine 134 13 6 6.1 West Virginia Young oak-hickory forest 137 10 5 6.1 West Virginia Second-growth mixed hardwoods 160 8 5 6.1 West Virginia Mountain hardwood forest 140 30 10 12.2 North Carolina Young oak forest 171 9 5 6.1 Virginia Upland oak-hickory 200 16 8 8.1 Connecticut Lower second-growth hardwood 134 12 8 6.1 West Virginia Upland oak forest 130 12 7 9.7 Virginia Upland oak-pine forest 148 10 8 9.4 New Jersey

Type D habitats

Mature mesophytic forest 342 20 8 6.1 West Virginia Virgin beech-maple forest 637 31 11 6.1 Ohio Oak-maple-hickory forest 321 19 6 6.1 West Virginia Lowland oak-beech-maple forest 440 26 10 8.1 New York Old growth oak-hickory forest 427 35 11 9.1 Indiana Mature northern hardwoods 256 25 9 12.2 West Virginia Mature mixed hardwood forest 384 20 9 7.7 Indiana Mature oak-hickory forest 204 12 4 6.1 West Virginia Deciduous floodplain forest 657 25 11 6.5 Virginia Mature hardwood forest 462 21 8 6.1 West Virginia

" Territorial males/40 ha

mat ter and fleshy fruits) are not very impor tan t in any habi ta t type, and show no clear trend.

The da ta concerning impor tance of specialist guilds are presented in Table 5. The only specialist guild regularly present in A habi tats is the ground insectivore guild, repre- sented by the eastern meadowlark (Sturnella magna). This guild increases in impor tance in type C and D habitats , due to replacement of the meadowlark b y several forest turdids and parulids. Undergrowth insectivores are most impor tan t in B habitats , a l though D habi tats a t ta in nearly the same density. High foliage insectivores increase f rom complete absence in A habi ta ts to numerical dominance in D habitats . Note that these habi tats suppor t nearly twice

the average density o f high foliage insectivores as are suppor ted in all guilds in A habitats.

The max imum in number of guilds seen in D habi tats is due mainly to the addi t ion of three impor tan t guilds in this habi ta t type. Trunk surface insectivores (picids and sittids), twig and branch insectivores (parids) and sallying flycatchers ( tyrannids) reach their peaks of impor tance in these habitats . Al though D habi tats have on the average only 2 more guilds than B habitats , this is because of the peak of impor tance of frugivore-insectivores in B habitats , which for the most par t drop out in forest habitats .

Once again, notice that variance in communi ty structure as measured by the coefficient of variat ion of relative im-

k

Table 2. Density, species richness, guild number and mean no. species/guild vs. successional stage

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Stage A B C D Level of signifi-

2-+s.d. CV b 2• CV 2• CV 2_+s.d. CV cance c

Density" 85.4• 6 2 . 8 216.7-+71.6 3 3 . 0 143.2• 22.8 Species no. 5.2• 2.2 42.3 15.4-+ 5.7 37.0 13.1• 6.5 49.6 Guildno. 2.3-+ 0.7 30.4 6.8_+ 1.9 27.9 6.6• 2.0 30.3 Species/guild 2.3• 0.9 39.1 2.3--+ 0.4 17.4 1.9• 0.5 26.3

413.0_+146.8 35.5 ** 23.4• 6.5 27.8 **

8.8• 2.1 23.9 ** 2.7• 0.9 14.8 *

" Territorial males/40 ha b Coefficient of variation = s.d./2 x 100 c . p < 0.05, **p < 0.01

Table 3. General• composition of communities

Stage A B C D Level of signifi-

2_+s.d. CV a 2• CV 2_+s.d. CV 2-+s.d. CV cance b

% general• 85.5• 12.0 14.0 56.7• t8.4 32.5 21.1 • 86.3 # general• sp. 3.7-+ 1.8 48.7 6.8• 2.3 33.8 3.0_+ 2.1 70.0 #gen. guilds 1.0-+ 0.0 0.0 2.7_ 0.5 18.5 2.1• /.0 47.6 #spec. spp. 1.5• 0.9 60.0 8.6• 5.1 59.3 10./-+ 5.7 56.4 # spec. guilds 1.3• 0.7 5/.9 4.1• 1.7 42.2 4.4_+ 1.4 32.5 2sp/guildgen. 3.7_+ 1.8 49.4 2.5_+ 0.6 24.0 1.2_+ 0.5 45.4 2sp/guild spec. 1.1_+ 0.5 45.2 2.0• 0.7 35.0 2.4_+ 0.9 37.5 % non-passerine 1.5-+ 3.6 240.0 3.6_+ 3.4 94.4 6./-+ 4.3 70.5

10.4• 87.5 ** 4.3-+3.0 69.8 ** 2.3-+1.3 58.2 **

19.1• 22.0 ** 6.4• 18.3 ** 1.5• 60.0 ** 3.0• 10.0 ** 7.0• 74.3 *

Coefficient of variation = s.d./2 x 100 b * p<0.05, ** p<0.0/

Table 4. Analyses of "general• guilds

Successional A B C stage

2• CV x i s .d . CV

D

2-+s.d. CV 2-+s.d. CV

Level of signifi- cance b

Omnivores

Species # 0.0-+ 0.0 0 1.2___0.8 % total density 0.0• 0 5.3• Density" 0.0 • 0.0 0 9.1 • 6.2

Graminivore insectivores

Species# 3.7-+ 1.8 48.7 4.3-+ 1.6 % total density 80.5 • 16.1 20.0 44.8 • 16.5 Density 69.3 • 34.6 49.9 90.4-+ 34.5

Frugivore-insectivores

Species# 0.0• 0.0 0 1.4-+ t.0 % total density 0.0-+0.0 0 6.4_+ 4.1 Density 0.0-+0.0 0 15.2•

66.7 0.8__+0.6 75.0 1.6+ 1.1 68.7 ** 81.1 4.1_____3.4 82.9 5.0-+ 4.0 80.0 ** 68.1 6.5__+5.4 83.1 24.0__+25.5 106.3 **

37.2 1.6__+ t.1 68.7 1.9--+ 1.6 84.2 ** 3 6 . 8 16.1__+17.5 108.7 4.3+ 5.0 116.3 ** 3 8 . 2 13.2__+10.5 79 .6 17.4__+16.6 95.4 **

71.4 0.2__+0.4 200 .0 0.4__+0.5 125.0 ** 64.1 0.6--+1.2 200 .0 0.9__+1.5 166.7 ** 79.6 0.9__+1.9 211.1 4.7--+8.5 180.9 **

a Territorial males/40 ha b * p<0.05, ** p<0.01

portance, density and species number of most guilds is generally lowest in type D habitats, reinforcing the contention that these habitats support communities which are more uniform in composition than those of early successional habitats.

Only nine guilds are individually analyzed in Tables 4 and 5 as these are the only guilds to show statistically significant differences among the four categories. Raptors, frugi- vores, nectarivore-insectivores, graminivores and aerial flycatchers are all either numerically unimpor tant in these habitats or inadequately censused by the spot-map method.

Discussion

Species richness and total density showed essentially the same pattern of change as reported by earlier studies (John- ston and Odum 1956; Kricher 1973; Shugart and James 1973; Karr 1968), although the pattern seen here is not shown in all studies. In contrast to the peak of species richness in older forest I found, Smith and MacMahon (1981) found a peak of species diversity in preclimax forest in Utah and Idaho.

Variance in species richness and density was highest in

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Table 5. Analyses of "specialist" guilds

Successional A stage

B C D

2_+s.d. CV 2• CV 2_+s.d. CV 2_+s.d. CV

Level of signifi- cance

Ground insectivores

% total density 8.5_+6.8 80.0 2.7_+ 3.3 122.2 species # 0.9_+0.6 66.6 0.7_+ 0.7 100.0 Density a 5.8_+4.5 77.6 5.9_+ 7.5 127.1

Undergrowth inseetivores

% total density 3.1• 6.9 222.6 13.7_+ 7.7 56.2 species# 0.5_+ 0.9 180.0 2.1_+ 0.9 42.9 Density 5.4_+14.6 270.4 30.7_+22.9 74.6

High foliage insectivores

% total density 0.0_+ 0.0 0.0 19.5_+11.8 60.5 species # 0.0• 0.0 2.9-+ 2.3 79.3 Density 0.0 -+ 0.0 0.0 43.0 -+ 29.4 68.4

Twig and branch insectivores

% total density 0.0_+0.0 0.0 0.5_+ 1.5 300.0 species # 0.0_+0.0 0.0 0.1_+ 0.3 300.0 Density 0.0 _0.0 0.0 0.7_+ 2.1 300.0

Trunk surface insectivores

% total density 0.0• 0.0 0.0• 0.0 species # 0.0 • 0.0 0.0_+ 0.0 0.0 Density 0.0__ 0.0 0.0 0.0 + 0.0 0.0

Sallying flycatchers

% total density 0.0_+0.0 0.0 3.4+3.2 94.1 species# 0.0• 0.0 1.3_+1.3 100.0 Density 0.0_+0.0 0.0 8.8_+8.8 100.0

26.3_+16.6 63.1 13.9_+ 8.8 63.3 ** 2.1___ 0.9 42.9 3.0+ 1.2 40.0 **

40.0_+31.6 79.0 50.8+29.0 57.1 **

5.2• 121.1 5.9-t-_ 5.2 88.1 ** 0.7___0.9 128.6 1.9+_ 0.7 36.8 ** 7.1_+8.5 119.7 26.7_+30.5 114.2 **

35.7__.15.9 44.5 38.5_+10.0 26.0 ** 4.4_+ 2.4 54.5 6.2_+ 1.9 30.7 **

45.5_+16.7 36 .7 156.0_+61.3 39.3 **

3.4_+3.7 108.8 5.9_+ 3.7 62.7 ** 0.7_+0.8 114.3 1.7_+ 1.1 64.7 ** 4.6_+5.5 119 .6 27.0_+22.4 83.0 **

2.6_+4.0 153.9 7.6+_ 4.4 57.9 ** 0.7_+0.8 114.3 3.3+_ 1.9 57.6 ** 3.9+5.7 146 .2 34.0+27.0 79.4 **

3.6• 138.9 15.4_ 7.3 47.4 ** 0.8_+0.9 112.5 2.6_ 1.1 42.3 ** 5.2+6.8 130 .8 63.2+30.7 48.6 **

" Territorial males/40 ha ** p < 0.01

early successional stages and reached a minimum in older forest. Whether this reflects differences in the magnitude of resource fluctuation cannot be determined from my data, but the high variance in density in A habitats contrasts with low variance in total density among sites in prairie bird communities seen by Wiens (1974). Wiens felt that low variance in density was caused by varying levels of productivity due to unpredictable climatic fluctuations ex- perienced by these communities. Prairie bird communities are thought to be unable to track resource fluctuations partly because of the lack of " refugia" to harbor subopti- really adapted populations during periods of resource stress; there is thus no pool of non-breeding individuals to colonize areas of high productivity and densities remain rather uniform despite widely varying levels of productivity. In contrast to prairie habitats, eastern grassland habitats are interspersed in mosaic fashion with other successional habitats which could serve as refugia allowing closer track- ing of resource levels by breeding populations during times of release from resource stress. Typical early successional breeding species such as the song sparrow and rufous-sided towhee were frequent breeding species in forest plots, although at much lower densities than those seen in early successional habitats.

Numerous researchers have found correlations between bird species diversity and various measures of vegetational heterogeneity such as foliage height diversity, percent vegetation cover, etc. (Karr 1968; Willson 1974; Shugart and

James 1973; Kricher 1973), although these correlations have not been found by all workers (cited in Holmes et al. 1979). In some studies it has been possible to identify exactly those changes in vegetation structure responsible for addition of bird species, and several of the trends shown by my data can be interpreted similarly. Willson (1974) and Holmes et al. (1979) found that the addition of trees to a habitat added species by providing a new foraging substrate, woody tissue. The same trend is shown here by the trunk surface insectivores and twig and branch insectivores, both of which reach maximum importance in older forest habitats. Most of these species are cavity nesters as well, further restricting their occurrence to habitats with trees.

Ground insectivores reach a peak of importance in forest stages also. This contrasts with Karr ' s (1971) find- ings, which showed a peak of ground foragers in earlier successional stages. Karr dealt with all ground foraging species however, not j~st insectivorous species. Patterns of detritus production and consequent changes in the litter fauna may account for the late successional peak in this guild, al though there is currently no information regarding this relationship.

Canopy insectivores also show a clear trend of increase with successional age, which is most likely related to the development of canopy vegetation. Aber (1979) has shown that in hardwood forests o f New Hampshire, formation of a concentrated canopy occurs at year 11 of succession,

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and that this canopy continues to grow upward through year 30. The canopy height varies predictably with age and is the major determinant of foliage height diversity.

Sallying flycatchers showed a marked increase in importance between younger and older forest, but it is not clear whether this is due to foliage structure or patterns of resource availability. Stiles (1980) found a similar pattern in alder forests of Washington and suggested that the closing of the forest midstory in mid-successional stages occluded space for sallying. Concentration of foliage into a single stratum occurs early in succession in New Hampshire forests (Aber 1979) and persists through year 30, when sub- canopy space presumably begins to open. Closed canopy forests in California support lower densities of flycatchers than open canopy forests (Beedy 1981), again suggesting the importance of open space to this guild. Holmes et al. (1979) made a similar suggestion.

Undergrowth insectivores showed a bimodal distribu- tion with peaks in shrub and older forest habitats. This suggests that their abundance is related to the amount of foraging substrate available, as shrubby vegetation is abundant in type B habitats. Forests show a reduced understory layer in early stages, with an increase in importance of understory vegetation in older forest (Aber 1979). Stiles (1980) however found that 2 species of understory foragers were lost from later successional stages in the sere he studied.

Several authors have predicted a change in feeding habits among the species inhabiting different segments of the successional gradient. Odum (1969) predicted an increase in specialization in later successional stages, and Ro- tenberry (1980) states that generalization in feeding habits is favored by high variability in habitat quality. Whittaker and Goodman (1979) suggest that species with a fluctuating carrying capacity (exploitation adapted) selection should favor opportunistic feeding habits, while species with a more stable K should reflect interactive selective pressures and show greater levels of adaptation to competition, presumably through ecological specialization. Pickett (1976) considers succession as the replacement of species in order of decreasing opportunism, i.e., early successional species are less specialized.

There is much circumstantial evidence that early successional habitats are in fact more variable in quality than later successional habitats. This is certainly true from the perspective of habitat persistence; the probability of a vege- tative community succeeding to the next stage is highest early in succession, i.e., the rate of change slows down as succession proceeds. Wiens (1976) points out that grassland vegetation dies back and regrows each season, and that variation in climate and production may be accompanied by spectacular variation in plant growth and pattern. He states that patch structure of woody vegetation and perhaps perennial plants in general is more stable than herbaceous or annual plants. As succession proceeds, Wiens further states, microvariations in environment may be buffered by the community structure. This could help to explain the lower patchiness of productivity in late successional habitats.

McNaughton and Wolf (1970) failed to find the predicted increase in specialization, stating that along a successional gradient bird species are equally specialized at each stage. The data presented here show a clear increase in specialist foraging guilds (as defined here) in later successional habitats. Although the definition of specialist used

here is rather broad, I would argue that a bird which eats only insects, even though it may eat a wide variety of types of insects, is more specialized than a bird which eats insects and a totally dissimilar food item such as seeds. The specialization in later successional habitats found here shows several components; a general decrease in the diversity of food items taken by the species inhabiting a given successional stage, addition of foraging specializations (guilds) within later successional habitats and an increase in the number of species per specialist guild in older forest habitats. Willson (1974) stated that species were added in later successional habitats mainly by the addition of guilds rather than the expansion of existing guilds.

Further evidence for increasing specialization is seen in the increase in importance of non-passerines later in succession. Klopfer and MacArthur (1959) noted a similar trend along a tropical-temperate gradient and attributed it to greater resource stability in the tropics. This allows increased abundance of non-passerines, which were assumed to be less flexible in feeding habits, and thus unable to exploit variable resources. Faaborg (1977) discussed the same phenomenon, and attributed it to the distributions of resources and metabolic rates of passerines and non- passerines. Many avian resources are lognormally distrib- uted, with an abundance of small items and paucity of large items. Passerines, with their higher metabolic rates, can out- compete non-passerines for the abundant small items due to higher activity levels, while non-passerines are superior at exploiting large items due to the lower energetic expense of harvesting them. This implies an increase in large, widely dispersed food items in later successional stages, and perhaps greater resource stability as well. Karr (1971) did not find the same consistent trend of increase in non-passerines with succession due to the abundance of non-passerines on his earliest successional plot.

A common inference from community based studies of resource partitioning has been that many communities are at a resource-limited equilibrium, and that competitive in- teractions have been important in structuring communities (Cody 1966, 1974; MacArthur 1958; Pianka 1978). Inten- sive studies of resource partitioning have demonstrated that foraging specializations by individual species often result in minimal overlap in resource utilization among coexisting species, particularly in forest communities (Schoener 1974). This reduction of overlap occurs both within guilds (Schoener 1974) and among guilds (Holmes et al. 1979). Wiens (1974, 1976), Rotenberry (1980) and Wiens and Ro- tenberry (1980) have argued that such resource based equilibria probably rarely occur in prairie grassland communities, due to unpredictable environmental fluctuations. Their studies fail to reveal the patterns of resource partitioning or ecomorphological patterns predicted by equilibrium- based competition theory. The avian communities they studied are quite similar to the herbaceous communities studied here, generally consisting of one Sturnella species plus one to several species of fringillids.

Kricher (1973) showed that temporal (week to week) variability in bird species diversity was highest in herbaceous plots, due to the sporadic influxes of non-resident species foraging opportunistically. Such variability was absent from later successional habitats. The implication from his study is that early successional breeding bird communities are not able to track resource fluctuations as readi- ly as later successional communities. The increased variance

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in community structure of early successional communities is supported by my data.

Competit ion for resources in communities at or near equilibrium would predict coadaptation over evolutionary time among coexisting species so as to minimize overlap in resource utilization. Such coadaptat ion however re- quieres a relatively stable composition of communities over evolutionary time. My data shows that variability in almost all aspects of community structure is highest in early successional habitats, and generally decreases as succession proceeds. Therefore, it is to be expected that tightly coadapted communities, if they do in fact occur, are most likely to be found in later successional habitats. Even within later successional habitats though, the amount of variance in community composition varies widely among guilds. For example, the lowest levels of variation are found within the high foliage gleaner guild. Interstingly, this guild has been the subject o f numerous studies indicating well-developed resource partitioning (MacArthur 1958; Williamson 1971; Roo t 1967; Rabenold 1978; Morse 1968). Willson et al. (1975) suggest that bark-drilling species might be sub- jected to resource limitation based on their data concerning patterns of dimorphism within these species. The insects fed on by these birds may be a more stable resource than other forest insect groups due to the microenvironmental buffering provided by woody tissue. Bark drilling species are mainly non-passerines, further suggesting a stable resource (Klopfer and MacArthur 1959).

In conclusion, patterns of resource utilization show consistent changes along a successional gradient, generally cor- responding with theoretical predictions concerning habitat or resource stability and ecological specialization. High variance in early successional community structure and a relative lack of foraging specialization in birds inhabiting these communities suggest that they may experience widely fluctuating environmental conditions which prevent attain- ment of equilibrium and the structuring effects of competition. Decreased levels of variance in community composition in later successional habitats as well as an increase in foraging specialization imply that these communities may more nearly approach the resource-based equilibrial conditions which could lead to structuring via interactive effects predicted by competition theory. Even within later successional habitats, however, resource based equilibria may be more frequent within some ecological groups (guilds) than in others.

Acknowledgements. This paper is derived from work originally conducted in partial fulfillment of the requirements for an M.S. degree at George Mason University. Many helpful comments were received on the original thesis manuscript from Carl Ernst and Larry Rockwood. Constructive criticism on other versions of the manuscript was provided by Peter Feinsinger, Carmine Lanciani, Jim Cohen, Jeff Lucas, and two anonymous reviewers. Special thanks to Jeff Lucas and Carmine Lanciani for assistance with computer work.

Appendix

Guild Classification

Abbreviations: R=raptor; G=graminivore; GI=ground insectivore; CI = canopy insectivore; AI = aerial insectivore; N-I = nectarivore-insectivore; TSI = trunk surface insectivore; SF1 = sallying flycatcher; O = omnivore; TBI = twig and branch insectivore; UI = undergrowth insectivore; FR-I=frugivore-insectivore; Fr=frugivore; Gr-I = graminivore-insectivore.

Buteo jamaicensis Buteo lineatus Buteo platypterus Falco sparverius Bonasa umbellus Meleagris gallopavo Colinus virginianus Phasianus colchicus Charadrius vocif erus Bartramia longieauda Philohela minor Zenaidura maeroura Coccyzus amerieanus Coccyzus erythropthalmus Tyto alba Otus asio Bubo virginianus Strix varia Caprimulgus carolinensis Caprimulgus vocif erus Chaetura pelagica Archilocus eolubris Colaptes auratus Dryoeopus pileatus Centurus carolinus Melanerpes erythrocephalus Sphyrapicus varius Dendrocopus villosus Dendrocopus pubescens Tyrannus tyrannus Myiarehus crinitus Sayornis phoebe Empidonax virescens Empidonax traillii Empidonax minimus Contopus virens Cyanocitta cristata Corvus brachyrhynchos Parus atrieapillus Parus carolinensis Parus bicolor Sitta carolinensis Certhis familiarus Troglodytes aedon Thryomanes bewickii Thryothorus ludovicianus Troglodytes troglodytes Mirnus polyglottos Dumetella carolinensis Toxostoma rufum Turdus migratorius Catharus mustelina Catharus guttata Catharus fusceseens Polioptila caerulea Bombyeilla cedrorum Sturnus vuIgaris Vireo solitarius Vireo griseus Vireo flavifrons Vireo olivaceous Setophaga rutacilla Dolichonyx oryzivorus Vireo gilvus Mniotilta varia Protonotaria citrea Helmitheros vermivorus Vermivora chrysoptera Vermivora pinus Parula americana Dendroica petechia

R R R R G G G G GI GI GI G CI CI R R R R AI AI AI N-I TSI TSI TSI TSI TSI TSI TSI SFI SF1 SF1 SF1 SF1 EF1 SF1 O O TBI TBI TBI TSI TSI UI UI UI UI Fr-I Fr-I O Fr-I GI GI GI CI CI Fr-I CI UI CI CI CI Gr-I CI CI CI GI CI CI CI CI

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Dendroica caerulescens CI Dendroica virens CI Dendroica cerulea CI Dendroica dominica CI Dendroiea fusca CI Dendroica castanea CI Dendroica pinus CI Dendroica discolor CI Seiurus aurocapillus GI Seiurus motacilla GI Geothlypis trichas UI Icteria virens UI Oporornis formosus GI Wilsonia citrina UI Wilsonia canadensis CI Junco hyemalis Gr-I Aimophila aestivalis Gr-I Sturnella magna GI Agelaius phoeniceus Gr-I Quiscalus quiscula Gr-I Molothrus ater Gr-I Icterus spurius CI Ieterus galbula CI Piranga olivaeea CI Piranga rubra CI Riehmondena cardinalis 0 Pheuctieus ludovicianus 0 Guiraca carulea Gr-I Passerina cyanea Gr-I Carpodaeus purpureus G Spinus tristis G Spiza americana Gr-I Pipilo erythropthalmus Gr-I Passerculus sandwichensis Gr-I Ammodramus savannarum Gr-I Passerherbulus henslowii Gr-I Pooecetes gramineus Gr-I Spizella passerina Gr-I Spizella pusilla Gr-I Melospiza georgiana Gr-I Melospiza melodia Gr-I

Breeding Bird Censuses Used in Analyses Figures indicate year, volume and issue of American Birds (or Audubon Field Notes) in which the census appeared, and census number.

Herbaceous plots : 1954, 8(6) : 29; 1955, 9(6): 23 ; 1968, 22(6) : 62; 1972, 26(6):85; 1975, 29(6):143; 1975, 29(6):146; 1975, 29(6):149; 1975, 29(6):152; 1977, 31(1):159; 1977, 31(1):161.

Herb, shrub and sapling plots: 1977, 31(1):162; 1955, 9(6):26; 1957, 11(6):17; 1958, 12(6):20; 1959, 13(6):23; 1961, 15(6):24; 1965, 19(6):38; 1967, 21(6):70; 1979, 33(1):82; 1981, 35(1):92.

Young forest plots: 1955, 9(6) : 6; 1955, 9(6) : 8 ; 1957, 11 (6): 7; 1958, 12(6):7; 1958, 12(6):8; 1959, 13(3):7; 1961, 15(6):12; 1964, 18(6) : 5; 1960, 14(6) : 11 ; 1973, 27(6): 43.

Older forest plots: 1969, 23(6): 13; 1974, 28(6):44; 1974, 28(6):16; 1974, 28(6):5; 1971, 25(6):25; 1971, 25(6):12; 1954, 8(6):13; 1957, 11(6):2; 1966, 20(6):11.

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Received April 19, 1982

secondary succession and breeding bird community structure: patterns of resource utilization

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