the adaptive syndromes of two guilds of insectivorous birds in the colorado rocky mountains

The Adaptive Syndromes of Two Guilds of Insectivorous Birds in the Colorado RockyMountainsAuthor(s): Robert C. EckhardtReviewed work(s):Source: Ecological Monographs, Vol. 49, No. 2 (Jun., 1979), pp. 129-149Published by: Ecological Society of AmericaStable URL: http://www.jstor.org/stable/1942510 .Accessed: 18/10/2012 00:44

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Ecological Monographs, 1979, pp. 129-149 ? 1980 by the Ecological Society of America

THE ADAPTIVE SYNDROMES OF TWO GUILDS OF INSECTIVOROUS BIRDS IN THE COLORADO

ROCKY MOUNTAINS'

ROBERT C. ECKHARDT2 Section of Ecology and Systematics, Cornell University, Ithaca, New York 14853 USA

Abstract. This paper analyzes the foraging behaviors of a community of insectivorous birds breeding in a high-altitude willow floodplain. The eight species belong to two guilds. Active searchers are represented by the gleaning guild (warblers): Wilsonia pusilla, Dendroica petechia, and Geothlypis trichas; passive searchers are represented by the fly-catching guild (flycatchers): Empidonax oberholseri, Empidonax traillii, Empidonax difficilis, Contopus sordidulus, and Nuttallornis borealis. The paper focuses on the following general questions: (1) What are the different components, and their correlations, of foraging behavior in the eight species? (2) What are the overall adaptive syndromes associated with predatory tactics of active and passive searchers? (3) Are the predictions of several models of optimal foraging supported by the results of the present study?

Adaptive syndromes (coordinated sets of characteristics, including the specific manner of resource utilization, and an array of other, related adaptations) are described for each species. Warblers forage primarily by gleaning, concentrating on stationary prey. Their velocity (average number of perches per minute) is ? 10.0, their search intensity (perches visited prior to an attack) is ?5.0, and their foraging intensity (number of attacks per minute) is >1.7. They have an attack radius (mean distance from perch to prey) of <0.6 m. Members of the gleaning guild may thus be characterized as active searchers (they look for prey difficult to find) but passive pursuers (they attack prey easy to catch). In addition, gleaners exhibit a narrow range of preferences in habitat structure. Flycatchers forage primarily by hovering or sallying, concentrating on prey available via aerial attack. They have both a velocity and search intensity of <4.0, and a foraging intensity of <1.8. They have attack radii ranging from 1 m to >7.5 m. Members of the fly-catching guild may thus be characterized as passive searchers (they look for prey easy to find) but active pursuers (they attack prey difficult to capture). Flycatchers show a broad range of preferences in habitat structure. For all species considered together there is an inverse correlation between body size and velocity, and a positive correlation between body size and attack radius.

Three core adaptations identify the adaptive syndromes of actively and passively searching predators. Active searchers have high velocities, high search intensities, and a foraging repertoire associated with passive prey. Passive searchers have low velocities, low search intensities, and a foraging repertoire associated with active prey. Additional characteristics also differentiate the two adaptive syndromes.

Search/pursuit ratios critical to numerous optimal foraging models are impossible to measure reliably in the field; thus the concept of active and passive searchers is proposed as a meaningful and readily quantifiable substitute. The data presented here exhibit poor fit with the predictions of several selected models. Predictions concerning differences in diet specialization, the extent of territorial and foraging overlap, and the prevalence of sexual dimorphism are not confirmed. In general, predictions concerning morphological size gradients are upheld; those concerning habitat specialization are confirmed if habitat is measured in structural terms, but are not supported when measured by vegetation type.

Key words: adaptive strategy; adaptive syndrome; Colorado, USA; community structure; flycatchers; foraging strategies; guild; insectivorous birds; optimal foraging; predation; pursuers; searchers; warblers.

INTRODUCTION

Ecologists have studied predation and predators from many points of view. One approach to predation is through modeling. The work of Lotka (1923) and his followers has inspired many models of optimal diet choice and numerous other predator responses to their prey (e.g., Holling 1959, Emlen 1966, Salt 1967, Rap- port 1971, Cody 1974a, Katz 1974, Pulliam 1974; also

1 Manuscript received 8 August 1977; accepted 4 July 1978. 2 Present address: Department of Zoology, Murray Hall,

University of Maine, Orono, Maine 04473 USA.

see the review by Schoener 1971). Another approach has been to search the literature widely for specialized types of data and, by comparing many different species of species groups, attempt to produce generalizations of widespread applicability (e.g., Schoener 1965, 1974, Hespenheide 1971, 1975a).

The exhaustive, single-species approach (e.g., Mu- rie 1944, Mech 1970) is classic and quite different, and has slowly led toward more comparative studies. Some studies still emphasize a particular species (e.g., Root 1967, Williamson 1971), while others concentrate on comparisons within and between local associations

130 ROBERT C. ECKHARDT Ecological Monographs Vol. 49. No. 2

of species that utilize the same resource base in similar ways (Cody 1968, Beaver and Baldwin 1975, Hespen- heide 1975b, Verbeek 1975). Such associations of functionally similar species are called guilds (Root 1967).

Although the species studied here are grouped in guilds, this paper is not about guilds per se. Rather, I use the guild concept as a means of isolating the different ways in which insectivorous birds capture their prey. Every species has associated with it a certain manner of resource utilization and a whole array of other, related adaptations. This "coordinated set of characteristics" has been termed an adaptive syndrome (Root and Chaplin 1976). Even though guild members may be distantly related taxonomically, their adaptive syndromes exhibit strong similarities. While Root and Chaplin (1976) confine the use of the term adaptive syndrome to a single species, I think it could be asserted that, broadly speaking, each guild has a single adaptive syndrome associated with it. Thus, members of a guild share the same adaptive syndrome, and the differences between members are relatively minor variations of secondary attributes of that syndrome. It follows, then, that a guild may be described as a set of species possessing the same adaptive syndrome, and exploiting a broadly similar resource base.

Because the term adaptive syndrome is relatively new, a brief comment upon it may be worthwhile. "Adaptive strategy" and adaptive syndrome are not equivalent terms. Unlike strategy, syndrome implies no grandiose plan nor direction toward a particular goal. The term adaptive strategy can have many different meanings. In contrast, adaptive syndrome has one precise meaning: the coordinated set of characteristics associated with an adaptation or adaptations of overriding importance, e.g., the manner of resource utilization, predator defense, herbivore defense, etc.

In this paper, I describe the adaptive syndromes of eight species of insectivorous birds. The birds are members of two guilds exemplifying two major types of prey capture: active searchers, represented by the gleaning guild (three species of Parulidae: Wilson's Warbler, Wilsonia pusilla; Yellow Warbler, Dendroi- ca petechia; and Yellowthroat, Geothlypis trichas), and passive searchers, represented by the fly-catching guild (five species of Tyrannidae: Dusky Flycatcher, Empidonax oberholseri; Willow Flycatcher, Empido- nax traillii; Western Flycatcher, Empidonax difficilis; Western Wood Pewee, Contopus sordidulus; and 01- ive-sided Flycatcher, Nuttallornis borealis). In addition, the study concentrates on the following general questions: (1) What are the different components, and their correlations, of foraging behavior in these eight species? (2) What are the adaptive syndromes associated with the feeding styles of active and passive searchers? (3) Do the predictions of several models of optimal foraging find support in the data presented here?

STUDY AREA

The study area, elevation 2658 m, lies at the lower end of Kawuneeche Valley, which contains the head- waters of the Colorado River and marks the western boundary of Rocky Mountain National Park. Situated 5.8 km north of the town of Grand Lake, Colorado, USA, at the junction of Onahu Creek and the Colorado River (at this point little more than a mountain stream), the study area is a small portion of extensive and continuous willow-scrub floodplain covering much of the floor of this glacial valley.

The dominant plants in the valley are shrubs grow- ing to a maximum height of =3.5 m. The two common species are both willows, Salix wolfii and Salix gey- eriana. Salix caudata, Betula glandulosa, bog birch, and Potentilla fruticosa, shrubby cinquefoil, are also present but in fewer numbers. Stands of willows are dissected by beaver channels, ponds, and dams, and are often bordered in wetter areas by sedges, in particular Carex aquatilis and Carex rostrata. Lodgepole pines, Pinus contorta, border the floodplain on both sides and can be found on higher ground among the willows as well.

A grid system was laid out in the study area, with 38-m intervals between markers; detailed physical and vegetation maps of the -35-ha area were drawn. The percent of each vegetation type within individual territories and in the overall study area was subsequently calculated by measuring the area covered by major plant types as indicated on these maps. The percent of the total study area covered by each vegetation type is illustrated in Fig. 3. Willows cover by far the greatest area (61%). Nearly one-third of the study area is occupied by sedges and expanses of water essentially unutilizable by members of the gleaning guild. The smallest area (9o) is covered by pines, which occur as isolated individuals, small stands, and peripheries of extensive forests that border the floodplain.

Four other localities in Rocky Mountain National Park were visited in 1975 to augment observations on species not well represented within the study area. Three of these sites are also in Kawuneeche Valley. (1) Onahu Creek, from its intersection with US Route 34 southward to the northern limit of the study area, winds for 2.2 km through habitat similar in all respects to the main study area. Here I made observations on all species, with particular emphasis on Yellowthroats and Olive-sided Flycatchers. (2) The same type of habitat is also found in the second area, near the junction of Squeek Creek and the Colorado River at an elevation of 2743 m. Here I observed only the foraging of Western Flycatchers. (3) The third site, around the Green Mountain Residential Area (National Park Ser- vice housing), adjoins the Onahu Creek study region north of the main study area, but is composed primarily of lodgepole pines with an open understory lacking in willows. Again I observed only Western Flycatchers. (4) In East Inlet Valley, east of the town

June 1979 ADAPTIVE SYNDROMES OF TWO AVIAN GUILDS 131

of Grand Lake, I made additional observations on Olive-sided Flycatchers. This fourth area, at 2620 m, is locally referred to as "second meadow," and lies -2 km east of the head of East Inlet Trail. The conifers here are somewhat more diverse than in the other areas: Englemann spruce, Picea engelmannii, and subalpine fir, Abies lasiocarpa, occur as well as lodgepole pine. Flycatchers appear to use these three tree species indiscriminately for perches and nest sites.

The weather of the study sites is unpredictable and harsh for birds attempting to breed. Snowstorms are possible in June after the arrival of migrants and can cause heavy adult mortality (Eckhardt 1977). The yearly average of snow and rainfall for the area is equivalent to -53 cm of rain, but the amount and distribution of rainfall during the summer are highly variable. The temperature, averaged May-August, is only 100C, and the onset of summer highs can vary by as much as 2 wk. In addition, snow accumulation during the previous winter varies widely, significantly influ- encing the degree and duration of flooding over the valley floor in the spring and early summer.

METHODS

Each field season, prior to the observation period, my assistants and I spent an average of 2 wk capturing birds with mist nets. To aid in territory measurement, each captured bird was marked with a unique combination of colored plastic and aluminum leg bands. In addition to bands, we attached small vinyl flags to the legs of Empidonax flycatchers in 1973. In nearly all cases, however, the flags were lost within the first few weeks after banding, and this procedure was aban- doned in subsequent years. In 1973, 28 of the 40, in 1974, 16 of 38, and in 1975, 12 of 39 territories under observation in the study area contained at least one banded individual.

Whenever possible, the sex of all birds captured and banded (a total of 138 for the six species breeding in the study area) was determined by observing for identifying plumage as well as the presence or absence of either a brood pouch or a cloacal protuberance; birds were then subjected to the following measurements: (1) wing chord, measured from the bend of the unflat- tened wing to the tip of the longest primary; (2) weight, measured on spring scales to the nearest 0.1 g; (3) bill length, taken from the bill tip to the posterior margin of the nostril; and (4) bill width, measured from one tomium to the other in the plane that passes through the posterior margins of both nostrils. Measurements were also taken on birds collected for a study of stom- ach contents in similar habitat in neighboring Arapaho National Forest. Because sample sizes were small in some species, measurements were also made on additional museum specimens collected during the breeding season from high-altitude Colorado, northern New Mexico, and southern Wyoming. I made an additional measurement on all museum specimens of (5)

tarsus length, measured from the posterior bend of the junction of the tibia and metatarsus to the junction of the first digit.

A total of 765 h was spent in observation during the following periods: 21 June-12 August 1973, 19 June- 6 August 1974, and 16 June-28 July 1975. Data collec- tion in the field was divided into two parts, foraging observations and determination of territorial boundaries. My assistants (different each year) mapped territories (a total of 376 h of observation for the three summers) by daily wandering, in random fashion, through a section of the study area. Usually all sections of the study area were visited before repeating a previously worked section. Except for movements necessary to identify individual birds by their bands or to confirm the exact perch of a singing male, pur- posive behavior on the part of the observer was minimal; birds were not followed or otherwise influenced to alter their response to territorial boundaries. Bird location and important behavioral events such as singing, chipping, foraging, fighting, etc., were recorded daily on cumulative maps for each territory. The final result is what Odum and Kuenzler (1955) term maximum territory, although I have slightly altered their method of observation to fit the circumstances.

I collected foraging and life history data during all three summers, totaling 389 h in the field. I attempted to cover different sections of the study area with equal frequency, and to observe each species for about the same length of time. Timed foraging observations total 2637 min for all species. Sums for individual species (in minutes) are as follows: Wilson's Warbler, 176; Yellow Warbler, 132; Yellowthroat, 48; Willow Fly- catcher, 721; Dusky Flycatcher, 417; Western Wood Pewee, 663; Western Flycatcher, 78; and Olive-sided Flycatcher, 381. I watched each individual bird as long as it remained continuously visible. For warblers, this usually meant no more than two observations of up to 15 or 20 s each. For flycatchers, observations might last as long as 1 min or so, very rarely as long as 15 min; however, the number of foraging movements per observation was generally < that for warblers.

Each observation was timed by stopwatch and recorded in a personal shorthand notation during or im- mediately afterward. Each entry included the following information: (1) date; (2) time at the conclusion of observation; (3) species; (4) sex; (5) individual color bands or other distinguishing features (such as song), if any; (6) location, to the nearest marker flag of the grid system if within the study area; (7) species of perch plant and condition of perch vicinity, either "dead" and without foliage or "live" and with foliage; (8) height of the perch plant; (9) height of the bird; (10) position of the bird, either on the periphery of the plant and exposed ("outside"), or in the interior of the plant and (usually) partly concealed ("inside"); (11) the number of times the bird changed perch and all distances between perches >1.5 m; (12) the length

132 ROBERT C. ECKHARDT Ecological Monographs Vol. 49, No. 2

of the observation to the nearest second; (13) whether or not the bird was singing, chipping, or interacting with other birds in any way; and (14) the details of all foraging movements.

I defined a foraging movement as any directed activity whose immediate purpose is the capture of a prey item. In this study, such movements were divided into four typesi gleaning, hovering, sallying, and pouncing. Gleaning is taking an exposed prey item from a solid substrate while the predator is perched. Hovering is taking an exposed prey from a solid substrate while the predator is actively flying, much as a hummingbird takes nectar from a flower. A sally (sometimes referred to as a "hawk") occurs when the predator leaves an observation perch, captures an air- borne insect on the wing, and returns to a perch. A pounce is a specialized form of sallying in which the predator alights on the ground only long enough to take a prey item. For each attack type I noted a specific set of information: for gleans, the total number during the observation and the substrate of each; for individual hovers, the distance and direction flown (up, down, or horizontal) and the substrate; for each sally, the distance and direction flown; and for each pounce, the distance flown (the direction is always down).

Unfortunately, I never was able to determine visually the prey items taken, or even to distinguish successful from unsuccessful attacks. Thus all foraging data is given simply in attacks without regard to success rate. In addition, adequate data are lacking on actual attack height for most of the eight species. In the Western Wood Pewee, however, the height of the initiating perch is a good approximation of the height of the actual attack (R. C. Eckhardt, personal observation), and this pattern appears to hold for all eight species. Thus I use perch height here as an indicator of attack height.

All measurements of foraging height and distance were judged by eye, with reference to study area grid markers for longer distances. Unless otherwise stated, in calculations and figures involving height and distance intervals I have lumped the data into 1.5-m intervals.

Except where otherwise credited, all statistical tests and methods are taken from Bishop (1966). Student's t test is used in all tests of significant difference between two means. Diversity is calculated using a standard measure, J, which corrects for the effects of different numbers of categories. The index is defined as H'/H'max, where pi is the

n proportion of the i-th category, H'= - pilog pi,

i=1

and H'max is the greatest possible value of H' having n categories, that is, when pi = 1/n for all i (Pielou 1969). Overlap values are calculated for pairs of

n species by the formula E min (pi, pj3), where pi,

x=1

is the proportional occurrence of species i in interval x (Colwell and Futuyma 1971, Feinsinger 1976). Both diversity and overlap values can range from a high of 1.0 to a low of zero.

As with any field methodology, there are a number of possible sources of error in the data presented here. Some of these difficulties and the ways in which I have dealt with them are discussed in the appropriate sections. A few of the more general problems deserve consideration here.

Territory data were collected by a different person in each of the 3 yr. I had assistants work on this data only because territory measurement is less susceptible to individual bias than foraging measurement or other types of observations I performed. Even though I was careful to require standard field methods and interpretation, individual differences were unavoidable. Thus all the information obtained from territory work is averaged over the 3 yr and used only to compare different species. No attempt is made to compare results between different years.

Mistakes in species identification can be a problem in any study of this sort. Female Yellow Warblers and female Wilson's Warblers are occasionally very similar in appearance. Male Empidonax flycatchers are indistinguishable in the field except by their song. Fe- males, which do not sing but give only infrequent call notes (at times species specific, at other times simply confusing), are thus often impossible to distinguish unless seen with an identifiable mate. To minimize the errors due to misidentification, I have eliminated all observations where species identity was in doubt.

Several other problems are inherent in the observation of foraging in small birds. As well as being easier to identify, males are often more conspicuous and more easily found and observed than females due to their territorial defense behavior. To reduce the possibility of over-representing male behavior, and to eliminate the complicating factors which singing bouts introduce into the calculations of total foraging times, I have, except where noted (Tables 6 through 9), used only those observations of foraging behavior alone ("nonsinging, period"). Otherwise, all observations which include any singing whatsoever ("singing period") have been disregarded.

Another difficulty is that in certain foraging areas, such as the interior of willow bushes and the tops of more densely foliated pines, it is more difficult to obtain reliable and complete observations than in a more open situation. Such an observational bias applies to all species, of course, and is only a problem should a particular species spend a relatively disproportionate amount of its time foraging in areas especially difficult for observation. In the present study, only Yellow- throat observations are probably biased in this way and for that reason, I spent proportionately greater time and care in my observations of Yellowthroats.

Finally, it is well known that breeding activity can


exert a strong influence on foraging behavior. Root (1967) documented that, in comparison with individuals engaged only in self-maintenance feeding, Blue- gray Gnatcatchers (Polioptila caerulea) attempting to feed both themselves and nestlings or fledglings showed the following differences in food gathering: (1) they spent a greater percentage of time foraging; (2) they had a greater frequency of attack maneuvers per unit of foraging time; (3) they increased the diversity of foraging maneuvers employed; and (4) they captured larger prey. Morse (1968) and C. P. Black (personal communication) report similar results in studies of warblers. Although in this paper I consider an average of foraging behavior over the entire breeding season, the reader should be aware that figures for any single phase of the breeding cycle may differ from the average. This aspect of the adaptive syndromes of gleaners and flycatchers will be explored in a subsequent paper.

THE GUILDS

A particularly useful way of approaching predation in insectivorous birds is by means of functional groups or guilds. Although it will always be possible to find a few species that fall between groups, a convenient division of avian insectivores might include: gleaners, which pick visually located insects from foliage and bark; sweepers, such as swallows and swifts, which prey upon the "aerial plankton"; flycatchers, which catch flying insects; woodpeckers, which utilize insects beneath bark and dead wood; and probers, such as creepers, which take insects concealed within cracks and crevices. In this study, sympatric members of two guilds are looked at in detail: gleaners, represented here by warblers, and flycatchers.

Three species that breed in the study area are members of the gleaning guild. The smallest of these (Fig. 1) is Wilson's Warbler, the most abundant bird in the study area. It builds a relatively bulky nest on the ground beneath willow bushes. The Yellow Warbler is larger and builds its nest in the upright crotches of willow bushes. The largest of the three is the Yellow- throat, which nests on or near the ground in dense tussocks of sedge. The breeding ranges of all three species overlap extensively in the boreal forests of southern Canada and the mountainous western portion of North America.

Three species that breed in the study area are members of the fly-catching guild. Two of these are sibling species in the genus Empidonax: the Dusky Flycatch- er and the Willow Flycatcher. The Dusky Flycatcher is the smaller of the two (Fig. 1); both species nest in forks or on horizontal branches in willows. The third flycatcher breeding in the study area is the Western Wood Pewee. Pewees build their nests far out on horizontal and frequently dead pine branches, usually those extending out over water. I have included in the local fly-catching guild two additional species that do

OLIVE-SIDED FLYCATCHER

WESTERN WOU, PEWEE | f l WI LL6W fLY ATCHER

WESTERN FLYCATCHER -t-- DUSKY FLYCATCHER

- - YELLOW WARBLER

-4- WILSON'S WARBLER

i- YELLOWTHROAT

60 80 100 WING LENGTH (MM)

OLIVE-SIDED FLYCATCHER WESTERN WOOD PEWEE

WILLOW FLYCATCHER WESTERN FLYCATCHER

OF DUSKY FLYCATCHER

+ YELLOWTHROAT

0 YELLOW WARBLER

4 - W. ILSON'S WARBLER

10 20 30 WEIGHT (GM)

FIG. 1. Weight and wing length of gleaners and flycatchers. Horizontal lines indicate the range of observed values, vertical lines designate the mean. Open rectangles enclose 1 SD above and below the mean, solid rectangles enclose the 95% confidence interval for the mean.

not breed in the study area proper. One of these, the Olive-sided Flycatcher, is by far the largest of the species studied. It places its nest high up in conifers, well concealed on live horizontal branches. The Olive- sided Flycatcher is an occasional visitor to the study area and nests in identical habitat adjacent to it. For this reason I include it as a full member of the guild. The final member of the fly-catching guild is yet another Empidonax, the Western Flycatcher. This species is not significantly different in size from the other two Empidonax. It inhabits open conifer woods bordering the willow floodplain, an area devoid of willows or other dense understory, and builds its nest on rock ledges or under cabin eaves. The Western Fly- catcher nests adjacent to the study area and on oc- casion is found within it. However, its usual habitat and nesting sites are sufficiently different from the other guild members that it qualifies for only ancillary membership in the local guild. For this reason, the species will at times be omitted from comparisons that seem inappropriate (e.g., those that require strict sympatry).

As with gleaners, the area of breeding range overlap for the five species of flycatchers is extensive, covering much of the western United States. Thus the patterns emerging from this study seem to be the product of extensive coadaptation, rather than the result of an unusual co-occurrence of species adapted to widely varying habitats and fellow guild members.


YELLOWTHROAT (39) [ o

YELLOW WARBLER (165) ___ __

W ILSON S WARBLER (427) _____ _____ _____ _____ _____ _____

glean - g hover sally-, pounce

DUSKY FLYCATCHER (58) I3

WILLOW FLYCATCHER (119) i0 0 ___

WESTERN FLYCATCHER (23) i_

WESTERN WOOD PEWEE (419)

OLIVE-SIDED FLYCATCHER (77) 0 50 100 I .I .I

percent FIG. 2. Foraging repertoires of gleaners and flycatchers; attack modes are illustrated as percentages of the total number

of attacks made by each species. Total number of attacks observed follows each species name.

Several other species that breed in the study area overlap in foraging habits to some degree with the eight species studied here. Lincoln's Sparrows, Mel- ospiza lincolnii, are common in the study area and have been observed from time to time to glean in dense growths of sedges and at the bases of willow clumps. However, such behavior represents only a small part of their foraging repertoire and occurs in parts of the

TABLE 1. Velocity, search intensity, and foraging intensity in gleaners and flycatchers. (n) = total number of observation periods.

For- Search aging

Velo- inten- inten- Species (n) city* sityt sityt

Wilson's Warbler (418) 33.3 9.7 3.1 Yellow Warbler (116) 25.0 5.0 4.6 Yellowthroat (29) 10.0 5.7 1.7 Western Flycatcher (43) 3.8 3.1 1.2 Willow Flycatcher (177) 2.9 3.4 0.8 Dusky Flycatcher (70) 2.6 2.7 1.0 Western Wood Pewee (264) 2.2 1.2 1.8 Olive-sided Flycatcher (133) 0.6 2.1 0.3

* Velocity is the average number of perches visited per minute, obtained by dividing the total number of perches by the total number of minutes in all observations.

t Search intensity is the average number of perches visited per attack, obtained by dividing the total number of perches by the total number of attacks in all observations.

t Foraging intensity is the average number of attacks per minute, obtained by dividing the total number of attacks by the total number of minutes in all observations.

vegetation rarely frequented by warblers. The suggestions of Cody (1974b, pages 97-98) notwithstanding, my own observations lead me to believe that Lincoln's Sparrows have diets clearly distinct from those of any of the gleaners studied here. Tree Swallows, Irido- procne bicolor, and Violet-green Swallows, Tachyci- neta thalassina, forage in the air space above the study area. While they probably overlap to some degree with flycatchers in prey taken, swallows usually forage higher above the willows and farther from the pine edges than even larger flycatchers under normal circumstances (cf. Hespenheide 1964). Because of differences in foraging methods swallows also take smaller prey (Hespenheide 1964, Holroyd 1975) from different taxonomic groups (Beal 1918, Hespenheide 1975a). Thus, although there are several species that may overlap in their foraging with some of the eight species examined here, the overlap is minimal and does not seriously obscure the distinctiveness of the two guilds as I have constituted them.

RESULTS

Modes of attack

Attacks directed at nonflying insects (i.e., gleans and hovers) constitute >90% of the foraging repertoire in all three gleaners, with sallies making up the remainder (Fig. 2). At least 75% of the attacks of a given gleaner species are gleans. The Yellowthroat gleans 97% of the time; and thus is the most restricted guild member in foraging modes utilized.

Forages for prey captured while the bird is in flight


(hovers and sallies) constitute 90o or more of the attacks made by the five species of flycatchers (Fig. 2). Among the Empidonax, both hovering and sallying predominate. In the larger species, sallies alone constitute well over 90%o of all attacks. Pounces are rarely employed, only with some frequency by Dusky Fly- catchers. The small Empidonax species exhibit the most diverse repertoires of foraging modes, while the largest member of the guild, the Olive-sided Flycatch- er, is entirely restricted to sallying.

Verbeek (1975) reports similar foraging behaviors in Western Wood Pewee and Western Flycatcher on the Hastings Reservation in Monterey County, California USA. Sallying is the dominant mode in the two species, comprising 98.7% of all attacks in the Pewee and 60.0o in the Western Flycatcher (Verbeek 1975). Unfortunately, Verbeek (1975) lumps hovers and gleans together, making closer comparisons impossible.

Gleaning involves little more than an extra jab of the bill; thus gleaners can be considered relatively passive pursuers. Sallying and hovering, in contrast, require large expenditures of energy per attack; therefore, flycatchers can be considered relatively active pursuers. One could then consider attack-mode frequencies as indicators of "activeness of pursuit." Similarly, the two characteristics to be considered next, velocity and search intensity, can be thought of as indicators of "activeness of search."

Velocity and search intensity

Velocity is the average number of perches visited per minute. A perch is defined as a single location, regardless of the direction the bird is facing or the placement of its feet. Only a change in location is a change in perch. Gleaners visit a large number of perches (? 10) per minute (Table 1). Larger species have lower velocities and hence spend more time on each perch. Flycatchers visit a distinctly smaller number of perches per minute (<4). As with gleaners, velocities are lower in the larger species. If all eight species are considered together, the inverse relationship between body size (measured as the cube root of the weight) and velocity is significant at the .1% level (correlation coefficient, r = .98).

Velocity measures the absolute speed of search, that is, the frequency of perch changes (with the resulting change in location of perceptual field or searched volume) per unit time. Search intensity, defined as the average number of perches visited per attack; measures the relative speed of search, that is, the frequency of perch changes with regard to foraging rate. Again, the two guilds can be distinguished by means of the search intensity of member species (Table 1). Gleaners have high search intensities, ranging from 5 to nearly 10 perches per attack. Flycatchers exhibit low search intensities, ranging from 1.2 to 3.4. In both guilds, the largest species have among the lowest

search intensities. Thus whether one judges by means of velocity or search intensity, gleaners are more active searchers, while flycatchers are more passive searchers.

To summarize, gleaners actively seek out prey: they search for stationary prey on leaves and twigs and move quickly and constantly through the vegetation. They can be characterized as gleaning at least 75% of the time, having a velocity of : 10 and a search intensity of ?"5. Thus they are active searchers (they look for prey difficult to find) but passive pursuers (they attack prey easy to catch).

Flycatchers, which might be described as "sit-and- wait" predators (Pianka 1971), move far less frequently, waiting for suitable prey to enter their field of view. They can be characterized as hovering or sallying at least 90o of the time (with sallies usually the predominant mode), with both a velocity and search intensity of <4. They are, then, passive searchers (they wait for prey easy to find) but active pursuers (they attack prey difficult to catch).

Foraging intensity

The average frequency with which attacks are made is indicated by foraging intensity, defined as number of attacks per minute. Although there is no clear pattern of foraging intensity within the two guilds (Table 1), it is apparent that, in general, active searchers have higher foraging intensities than passive searchers. Pos- sible reasons for this include (1) the energetic costs of attack; (2) the rates of successful attack; (3) size of the bird and its metabolic rate; or (4) energetic return per prey item.

Vegetation preferences

Major preferences in vegetation type are expressed by the choice of habitat. In patchy habitats such as the one studied here, it may be possible for species to exhibit greater selectivity by means of territory placement, whereby individuals avoid areas of unfavored plants and locate territories in preferred vegetation. The composition of the average territory for each study area species is shown in Fig. 3 and can be com- pared with the average composition of the entire study area. Willows are by far the dominant vegetation type in both the study area and individual territories, while small percentages of sedges, open water, and conifers make up the remainder. Only in Yellowthroats (with 30% sedge) and Western Wood Pewees (with 22% pine) is there any noticeable departure from the general composition of the study area, but even that is not a great deviation.

Thus only two species show any sign of selectivity in territory placement. This is surprising, if only because one would expect that species with relatively small territories, such as Wilson's Warblers and Dus- ky Flycatchers (Table 4), are better able to adjust territorial boundaries to vegetation patterns and prefer-

136 ROBERT C. ECKHARDT Ecological Monographs Vol 49 No. 2

WILSON'S WARBLER _

YELLOW WARBLER _

YELLOWTHROAT I

WILLOW FLYCATCHER_

DUSKY FLYCATCHER |

WESTERN WOOD ! PEWEE *. *.;


WETRNFYCTHE________________________________ WESTERN FLYCATCHERS

willow - pine sedge air water

STUDY AREA 1 0 50 100 I .I .I

percent

FIG. 3. Vegetation utilization in gleaners and flycatchers. For each species: top bar, territory composition; middle bar, perch substrates; lower bar, attack substrates. See text for method of determining territory composition (no data for Olive-sided and Western Flycatchers). Perch substrate is the percent of the total number of attacks initiated from each type of perch for each species. Attack substrate is the percent frequency of attacks directed at each substrate out of the total number of attacks made by each species.

ences than species with relatively large territories, such as the Pewee and Yellowthroat. There are several possible explanations for this result. One is that measurement of maximum territory may not be sufficient to discern small-scale selection for vegetation type. Measurement of utilized territory (Odum and Kuen- zler 1955), that is, those parts of the maximum territory that are actually used as well as defended, may be necessary to provide a more accurate answer to the question. R. B. Root (personal communication) has suggested a corollary interpretation: territories of these species may include some minimal or average amount of preferred vegetation or foraging substrate, and the remainder is simply ignored. If this were so, measurement of the vegetative composition of territories would not reveal species preferences. Such "ignored segments" of territory could be a serious problem in studies employing foliage profiles determined from random points, etc. Another possible explanation is that these species do not exhibit vegetation preferences on a scale corresponding to territory size. Rath- er, it may be that microhabitat preferences within the habitat are expressed by means of behavior patterns,

WILSON'IS WARBLER :.::

YELLOW WARBLER ::.

YELLOWTHROAT ...... ' catkins foliage b bark A

live dead WILLOW FLYCATCHER

DUSKY FLYCATCHER

WESTERN WOOD PEWEE

OLIVE-SIDED FLYCATCHER I I

WESTERN FLYCATCHER

0 50 100 I .I .I

percent

FIG. 4. Perch and attack substrates by plant part in gleaners and flycatchers. For each species: upper bar, perch substrates; lower bar, attack substrates. Perch and attack substrate defined as in Fig. 3.

perch preferences, and selectivity for certain prey items.

Perch preferences

Gleaners and flycatchers may initiate attacks from a variety of live or dead perches, including willows, conifers (pine, spruce, or fir), or sedges. Gleaners show a marked partiality for willow perches, while flycatchers vary more in the frequency with which they use willow or coniferous perches (Fig. 3). The Empidonax breeding in the study area exhibit a tran- sition in preferences between the gleaners and the larger flycatchers which prefer coniferous perches. The habitat of the Western Flycatcher provides little opportunity for the use of willow perches, thus that species shows a marked preference for coniferous perches in contrast to its congeners. Sedges are rarely used, and then only by Wilson's Warblers.

The difference between the two guilds in the use of live and dead perches is quite distinct (Fig. 4). Live perches support live foliage and are usually surround- ed by other leafy branches. Dead perches support no foliage of their own and usually are devoid of foliage in the immediate vicinity. Gleaners show a strong preference for live perches (?79% of all perches). How- ever, flycatchers prefer dead perches (?63%), for here visibility of flying insects is better and aerial maneuvers are easier.

Attack substrates

The frequency with which prey from different substrates are attacked is a direct result of the attack modes used. Gleaners attack prey on solid substrates >90% of the time, and concentrate most of these at-



ZZZZZZ*ZZZZZZZZ I WESTERN WOOD PEWEE

WESTERN FLYCATCHER

WILLOW FLYCATCHER

DUSKY FLYCATCHER

WILSON'S WARBLER

YELLOW WARBLER

YELLOWTHROAT

0 3 6 9 12 15 18 DISTANCE (M)

FIG. 5. Attack radii in gleaners and flycatchers. Attack radius is the mean distance travelled from perch to prey. Explanation of symbols as in Fig. 1.

tacks on willows (Fig. 3). Only Wilson's Warblers prey on aerial insects to any degree, or attack insects on sedges at all. Flycatchers most frequently attack aerial insects. The smaller Empidonax utilize insects found on a wide range of other substrates as well, and each species has a different secondary attack substrate (willows in the Willow Flycatcher, sedges in the Dus- ky Flycatcher, and conifers in the Western Flycatch- er). In the two largest species, aerial forages constitute ?94% of all attacks.

When attacks on prey from solid substrates only are considered, members of both guilds concentrate on foliage insects (Fig. 4). Except for the Western Fly- catcher, no species directs >9% of its attacks to branches or twigs.

Attack radius and direction

The types of attack maneuvers employed also influence the average distance travelled from perch to prey. I call this distance the attack radius; it is calculated as the mean for all attacks in all four modes, including gleans (for which the distance traveled is defined as zero). Attack radii are shown graphically in Fig. 5. Comparisons between all pairs of radii are significantly different at the 1% level or better, except for the comparison of Yellowthroat with Yellow Warbler, and Western Flycatcher with the other two Empido- nax. There is a slight increase in attack radius with decreasing body size in gleaners, probably due to the similarly slight increase in aerial foraging in the smaller species. In flycatchers, there is a distinct increase in attack radius with increasing body size, resulting from the longer distances flown in aerial attacks by the larger species. If all eight species are considered together, there is a significant, positive correlation at the .1% level (r = .98) between average attack radius and size (cube root of the weight) of each species.

To demonstrate the shape of the volume searched by each species, a simple measure of the direction of

34

64 4-w1.5 WILSON'S WARBLER 2

29 0.9

64 *1 * 5 YELLOW WARBLER 7 \.

24 i

4 ,71.2

19 >57 4\?.9 DusKY FLYCATCHER

19 \1.6 22 1.6

74 2.4 WESTERN FLYCATCHER 4 0.6

21 1.8

<66 < 2.1 WILLOW FLYCATCHER 13 2.7

13 /5.2 252 4.4 WESTERN WOOD PEWEE

11 \3.1 56 9.7


38

5.7

PERCENT TOTAL MEAN DISTANCE (M) NUGER OF ATTACKS

FIG. 6. Aerial foraging vectors in gleaners and flycatchers. Arrows indicate attacks made in an upward, horizontal, or downward direction. Left-hand vectors illustrate the percent of the total number of attacks for each species in each direction. Right-hand vectors illustrate the average distance flown (in metres) in each direction.

aerial foraging attacks (either horizontal, upwards, or downwards) is graphically represented in Fig. 6. In all species, the predominant aerial foraging direction (and hence the preferred search focus) is horizontal; between 52% and 74% of attacks are in that plane. For gleaners, all but a very small percentage of the re- maining attacks are directed upwards. Because foliage insects are commonly found on the undersides of leaves, it is to a gleaner's benefit to direct a significant portion of its attention overhead. Among the flycatchers, the direction of attack preferred after horizontal depends on the size of the bird. Empidonax flycatchers exhibit a preference for upward flights, while the larger flycatchers prefer downward flights. Two possible reasons for this might be: upward flights are too expensive energetically for the larger flycatchers, or preferred prey are more abundant above the low perches used by small flycatchers, but below the high perches used by large flycatchers. The average distance flown in each direction is also shown in Fig. 6; horizontal flights are, with one exception, longer than those in any other direction.


YELLOWTHROAT

2L 15 0 3 PREY DISTANCE (M)

12- 12

WILSON'S WARBLER YELLOW LU 6 6 tWARBLER

6 3u6

0 3 6 9 0 3 6 PREY DI STANCE (M) PREY DI STANCE (M)

FIG. 7. Foraging space in gleaners. Foraging space is illustrated here by frequency of attacks by height and distance from the perch. Contour lines enclose areas of equal relative frequency of attack for each species. Lower contour values indicate lower relative frequencies. Calculations are based on 1-rn horizontal and vertical interval scales.

Verbeek (1975) measured the foraging vectors of Western Flycatchers and Western Wood Pewees in California and found distinctly different behavior from that reported here. In his study horizontal flights are

the least common. In the pewee, Verbeek (1975) reports that descending flights are most common (51%), followed by ascending (32%) and horizontal (17%). In the Western Flycatcher, ascending flights predominate (47%), then descending (29o), and finally horizontal (24%). The differences between Verbeek's (1975) and my data may be due to responses to the widely dif- fering types of vegetation found in the two study lo- cations, but they may also result from a more strict definition by Verbeek (1975) of horizontal flight.

Foraging space

The way physical space is utilized in foraging depends on the attack modes used, distribution of available prey, and types of prey preferred. Frequency distributions of distance of attacks from the initiating perch and the height of those attacks can be combined to create a three-dimensional representation of that foraging space. The result (Figs. 7 and 8) is similar to topographic map: regions of high attack frequency are portrayed as hills with contour lines of high relative value.

Gleaners concentrate most of their attacks in a core area extending 1.5 m horizontally from the perch and vertically from the ground (Fig. 7), and have relatively small total foraging spaces. Larger foraging areas are associated with smaller body size, probably because smaller species include a small percentage of sallying in their foraging repertoires (Fig. 2). Flycatchers, however, have relatively large foraging spaces (Fig. 8), and

12

W I LLOW 9 FLYCATCHER 9 1

6- 66 \- u ~~~~~~~~~~~~~~~~DUSKY

i: FLYCATCHER 21 i

3 2

18.

O 3 6 9 12 0 3 6 PREY DISTANCE (M) PREY DISTANCE (M) 2

15' 15-

12 12 ~12-

9 WESTERN 9 WOOD PEWEE2

'i all, ~WESTERN FLYCATCHER

6 ~~~~~~~~~~~~2 6-

OLIVE-SIDED 3 FLYCATCHER

3 3 3-

O. 0~ 04 0 3 6 9 0 3 6 9 12 15 0 3 f 2 1 21 PREY DISTANCE (M) PREY DISTANCE (M) PREY DISTANCE (M)

FIG. 8. Foraging space in flycatchers. For explanation see Fig. 7.


larger foraging area is associated with larger body size. This may be a product of several factors, including the increased sallying performed by the larger species (Fig. 2), and their characteristically greater attack radii (Fig. 5). Like gleaners, Willow and Dusky Flycatchers concentrate most of their attacks close to the perch and near the ground. Western Wood Pewees also have a core foraging area, but it is much larger. There are three preferred areas in the foraging space of the 01- ive-sided Flycatcher; these correspond to the regions extending from the tops of conifers of the three predominant age classes found in the study sites. Western Flycatchers, which forage in a somewhat different habitat, commonly attack higher off the ground and from a greater variety of heights than the other two Empidonax.

Morphology

The size and shape of the bill in birds are frequently used as an indicator of the size and type of prey taken (Keast 1972, Schoener 1974), and bill differences are commonly assumed to be a mechanism of resource partitioning (Schoener 1965, Johnson 1966). The ways in which prey are taken certainly define general bill morphology (Karr and James 1975), but they also determine those dimensions along which differentiation is most critical for ecological separation, what could be called the active dimensions. For example, warblers have long, narrow, rather needlelike bills with which they pluck insects and probe leaf and needle clusters and willow catkins. For this type of foraging, bill width is not as important a dimension as length. Consequently, the three members of the gleaning guild do not differ significantly in bill width, yet they differ significantly (at the 1% level) in bill length (Fig. 9). Bill shape, as measured by the ratio of bill width to bill length, is also significantly different (at the 5% level), but this is, in a sense, simply an artifact of the differences in bill length. (All tests by extended Tukey procedure; Spj0tvoll and Stoline 1973.)

In flycatchers, which commonly take highly active, aerial prey, the gape of the open bill (i.e., product of both bill length and width) is critical since it deter- mines the size range of prey and also sets limits to errors of judgment and skill during an attack. A larger gape thus results in larger potential prey and in greater possible deviations from a "direct hit" that still yield a successful capture. Figure 9 shows that flycatchers separate out in both active dimensions of bill length and width. If we exclude the Western Flycatcher, all differences are significant at the 5% level (extended Tukey procedure; Spj0tvoll and Stoline 1973). Bill shapes, as indicated by the width-length ratio, are not significantly different in any but a few extreme cases. Thus, while gleaners are differentiated on the basis of bill length, flycatchers can be distinguished by bill length and width.

OLIVE-SIDED FLYCATCHER WEST. WOOD PEWEE

- --i WILLOW FLYCATCHER

-~---- WESTERN FLYCATCHER -$2------@ - DUSKY FLYCATCHER

-- YELLOWTHROAT

- +-- YELLOW WARBLER - C WWILSON'S WARBLER

5 II 1 1:3 15 BILL LENGTH (MM)

OLIVE-SIDED FLYCATCHER WESTERN WOOD PEWEE E

WILLOW FLYCATCHER WESTERN FLYCATCHER

- '----' DUSKY FLYCATCHER -*--- YELLOW WARBLER

WILSON'S WARBLER YELLOWTHROAT

3 5 7 9 BILL WIDTH (MM)

WESTERN FLYCATCHER - Ei

WESTERN WOOD PEWEE WILLOW FLYCATCHER =

OLIVE-S. FLYCATCHER DUSKY FLYCATCHER l

e * | WILSON 'S WARBLER-

YELLOW WARBLER

- 1----- YELLOWTHROAT

.30 .50 .70 RATIO BILL WIDTH/LENGTH

FIG. 9. Bill dimensions in gleaners and flycatchers. Ex- planation of symbols as in Fig. 1.

Another possible method of resource division, sexual dimorphism, was tested; several different morphological features were measured for each of the eight species (Table 2). All species are dimorphic in wing length. In addition, female Wilson's Warblers have a greater bill width and a larger bill width/length ratio than males; in Yellow Warblers, males have longer tarsi than females; and among Dusky Flycatchers, males weigh more than females. Thus consistent patterns of sexual dimorphism occur only in coloration (warblers are dimorphic, flycatchers are monomorphic) and wing length (uniformly dimorphic in both guilds). Why wing length is consistently dimorphic, but body weight is, with one exception, monomorphic, is a puzzle. While this pattern suggests that wing dimorphism is due to sexual differences in the demands of flight, just what those differences might be is not at all obvious. Males of the eight species studied do not perform conspicuous or elaborate aerial courtship displays, and it does not appear that they fly greater distances during migration than females. Perhaps another, undetermined difference in flying behavior is responsible.


TABLE 2. Sexual dimorphism in gleaners and flycatchers. Means + standard error. Comparisons by two-tailed t tests.

Bill Wing Bill Bill ratio

Species length (mm) Weight (g) Tarsus (mm) length (mm) width (mm) width/length

Wilson's Warbler d 57.9 ? .2 7.96 ? .05 15.3 ? .2 7.06 ? .06 3.48 ? .03 .497 ? .006 **56.0 .2 8.38 ? .26 15.5 ? .2 7.11 ? .10 3.66 ? .05 .516 ? .006

d 62.5 ? .3 8.56 ? .37 15.0 ? .2 8.43 ? .08 3.58 ? .05 .426 ? .006 Yellow Warbler )y **59. 1 .4 8.97 ? .13 14.0 ? .2 8.20 ? .12 3.58 ? .05 .435 ? .006

d 55.7 ? .5 16.1 ? .3 8.71 ? .08 3.56 ? .05 .409 ? .007 Yellowthroat ?y **53.8 .2 16.0 ? .3 8.46 ? .10 3.40 ? .07 .390 ? .130

d 69.6 ? .4 12.0 ? .5 14.9 ? .2 9.17 ? .10 5.13 ? .07 .564 ? .007 Dusky Flycatcher )y **66.6 ? .5 10.9 ? .2 14.6 ? .3 9.09 ? .06 5.11 ? .09 .561 ? .008

d 70.9 ? .4 13.6 ? .2 9.6 + .1 6.05 ? .05 .628 ? .008 Western Flycatcher So **64.6 ? .7 13.0 ? .4 9.6 ? .2 5.87 ? .11 .614 ? .019

Willow Flycatchrd 71.0 ? .3 13.9 ? .2 10.1 ? .1 6.05 ? .07 .604 ? .006 Willow Flycatcher Y) **67.9 ? .8 13.8 ? .3 10.2 + .1 6.12 + .07 .598 ? .006

d 88.0 ? .3 13.2 ? .3 10.3 ? .1 10.8 + .1 6.65 ? .04 .616 ? .007 Western Wood Pewee )y *84.9 ? 1.3 18.5 ? 3.5 10.4 ? .2 10.5 ? .2 6.60 + .16 .630 ? .009

Olive-sided Flycatcher d 108.5 ?

.6 33.5 ?

.7 11.3 ?

.2 15.0 + .2 8.81 + .07 .589 ?

.007 F *104.6 ? 1.6 34.2 + .8 11.3 ? .5 14.6 + .3 8.81 ? .11 .605 ? .014

* Difference significant at the 5% level. ** Difference significant at the 1% level. t Insufficient data.

Diversity patterns

Birds differ not only in the choice of plant species for perch sites and attack substrates, but also in the variety or diversity of their preferences. This diversity can be calculated using a standard diversity measure, J, which quantitatively reiterates some of the preced- ing generalizations (Table 3). Both guilds display considerable variation and overlap in diversities of attack modes and vegetation preferences for perch and prey substrates. However, when structurally oriented behavior is considered (perch and attack height, attack distance), flycatchers have consistently more diverse preferences than gleaners.

Territorial overlap

The way a species responds to other members of its own guild can be contrasted with its response to members of other guilds to suggest how the adaptive syndromes of species and guilds interact. The six species breeding in the study area frequently come into contact with one another, and their territorial boundaries are largely a resolution of such contacts and possible conflicts. The extent of territory overlap among different species is one measure of their response to one another as potential competitors.

Table 4 summarizes the extent of territory overlap among the six study area birds. Overlap is calculated as the mean of the areal sums of overlaps on individual territories, and is expressed as a percentage of the mean territory size of each species. As one might expect, intraspecific territorial overlap is generally small (column 1). Only Wilson's Warblers have a significantly larger number of intraspecific

overlaps (P < .001), in contrast to the other species whose numbers are far lower than possible when judged by spatial constraints alone. Wilson's Warblers (by far the most abundant species) probably approach the limit of the number of territories possible within the study area. Thus, while most of the other species' territories are widely spaced, Wilson's Warbler territories frequently share common boundaries or overlap with conspecifics. The amount of overlap with other species of the same guild (column 2) is strikingly uni- form in the two guilds, ranging from 25% to 44%. Overlap with members of the other guild is, on the whole, much larger, ranging from 30% to 108%. What this suggests is that, in terms of interspecific territo- riality, selection has resulted in behavior reflecting the fact that other species belonging to the same guild of a certain species are greater potential competitors than species belonging to different guilds. For a given species, then, territorial overlap is greater with species of different guilds, even closely related ones, than it is with species of the same guild, or with conspecifics.

DISCUSSION A synthesis of optimalforaging models

Over the last 15 yr, many ecologists have contrib- uted to the body of theory outlining feeding strategies and optimal foraging in predatory species (among them MacArthur and Levins 1964, Emlen 1966, MacArthur and Pianka 1966, Schoener 1969a, 1969b, 1971, MacArthur 1972). Different workers have chosen a variety of properties to be optimized, maximized, or minimized, and a variety of ways to measure them. Many theories concentrate on a set of characteristics


TABLE 3. Diversity indices (J) for selected traits in gleaners and flycatchers.

Mode Attack Perch Perch Attack Attack Species of attack* substratet substratet height#? heightt distance:

Wilson's Warbler .66 .69 .54 .55 .56 .14 Yellow Warbler .33 .44 .47 .56 .58 .06 Yellowthroat .19 0.0 0.0 .63 .48 0.0

Dusky Flycatcher . .72 .91 .99 .80 .65 .70 Willow Flycatcher .56 .65 .87 .68 .66 .59 Western Flycatcher .93 .75 .44 .89 .92 .71 Western Wood Pewee .23 .19 .76 .84 .74 .74 Olive-sided Flycatcher 0.0 0.0 0.0 .91 .86 .90

* Data from Fig. 2. t Data from Fig. 4. t Calculated with 1.5-m interval groupings. ? As measured by the number of nonsinging perches, regardless of whether an attack is made or not.

which can be visualized as a continuum (of which there are many, e.g., large/small, specialist/generalist, searcher/pursuer) and predict the optimal solutions to evolutionary or ecological problems that the two extreme ends of the spectrum should display. In spite of a great variety of methods, purposes, assumptions, and results, these models often display a comforting uniformity and complementarity of predictions. If these conclusions are synthesized into a logical, uni- fied set, the result is a theoretical description of adaptive syndromes that is particularly relevant to an understanding of the gleaning and fly-catching guilds.

One approach to optimal foraging appropriate to the present study is to divide predators into searchers and pursuers (MacArthur and Pianka 1966, Schoener 1969a, 1971, MacArthur 1972). This approach assumes that predators lie along a continuum bounded on one end by species that spend all of their foraging time or energy in search, handling, and swallowing of prey and none in pursuit (i.e., pure searchers); the other end of the continuum is bounded by species that spend all of their foraging time or energy in pursuit, handling, and swallowing of prey and none in search (i.e., pure pursuers) (MacArthur and Levins 1964, Schoener 1969a). Even though neither extreme is very realistic (Schoener 1969a), conclusions are usually drawn concerning pure searchers and pure pursuers. In the following paragraphs I summarize some of the general-

izations and predictions proposed for searchers and pursuers, and some others relevant to the synthesis. The reader may refer to the original works cited for a more detailed discussion of the background and logic of each conclusion.

Searchers are defined as those predators with a high ratio of

time (or energy) spent in search time (or energy) spent in pursuit

(MacArthur and Pianka 1966). (Pure searchers, whose ratio has a denominator of zero, are equivalent to Type II predators of Schoener [1969a].) Pursuers, however, have a low search/pursuit ratio (and pure pursuers, whose ratio has a numerator of zero, are equivalent to Type I predators of Schoener [1969a]). MacArthur and Pianka (1966) hypothesize that pursuers should be "'more restricted in diet," while searchers should be less restricted (see MacArthur 1972). Schoener (1969a) suggests more specifically that pursuers should exhibit a narrow range of prey sizes taken, while searchers should exhibit a broad range of prey sizes (in Schoe- ner's (1969a) model, size was the only criterion for prey choice). Thus both works predict that searchers should be diet generalists, while pursuers should be diet specialists. MacArthur and Levins (1964) take the idea one step further and propose that diet specialists are habitat generalists, and diet generalists ("species

TABLE 4. Average total area of territorial overlap and mean territory size. Overlap is calculated as the mean of the areal sums of overlaps on individual territories, and is expressed as a percentage of the mean territory size of each species.

All other Mean Individuals of individuals of All individuals of territory size

Species the same species the same guild the other guild (ha ? SE)

Wilson's Warbler 23 39 71 .31 ? .02 Yellow Warbler 4 44 73 1.89 ? .28 Yellowthroat 0 41 55 2.20 ? .66

Dusky Flycatcher 1 42 100 .73 ? .23 Willow Flycatcher 2 33 108 1.72 ? .35 Western Wood Pewee 0 25 30 1.70 ? .39


TABLE 5. An outline of searcher-pursuer theories. See text for sources.

Pursuers Searchers

low search/pursuit ratios; Type I high search/pursuit ratios; Type II of Schoener (1969a) of Schoener (1969a)

1. diet specialists with narrow range of food sizes and 1. diet generalists with wide range of food sizes and types. types.

2. habitat generalists. 2. habitat specialists. 3. overlapping territories (home ranges) or foraging 3. nonoverlapping territories (home ranges) or foraging

sympatry with other pursuers. allopatry with other searchers. 4. differ from other species in body size (by 4. not distinctly different from other species in body size.

Hutchinsonian distance). 5. sexual dimorphism present. 5. sexual dimorphism absent. 6. many species packed along a linear resource 6. few species packed along a linear resource gradient.

gradient.

which specialize on a particular proportion or mixture . . .resources") are habitat specialists. Sympatric species of pursuers should then have territories or home ranges covering a variety of habitats or microhabitats and should overlap considerably with each other (because each species specializes on a particular prey). Sympatric species of searchers should have relatively nonoverlapping territories or home ranges covering a fairly limited number of different habitats or microhabitats. Similarly, Schoener (1969a) suggests that searchers will exhibit foraging allopatry with other searchers (except where food is very abundant), while pursuers will exhibit foraging sympatry with other pursuers.

MacArthur and Levins (1964) predict that sympatric pursuers will be separated by "coarse-grained differences" in morphology. Because differences in diet are often manifest in gradations of bill or body size (Schoener 1965, 1974, Keast 1972), pursuers should differ in bill or body dimensions, possibly by the "Hutchinsonian distance," that is, by multiples of 1.14 or more (Hutchinson 1959, Schoener 1965). Sym- patric searchers, however, should not be distinctly different in either bill or body size (MacArthur and Levins 1964). In addition, Schoener (1969a) predicts that sexual dimorphism is more prevalent among pursuers than among searchers. Finally, it is suggested that in a single community, and along a resource gradient such as food, more species of pursuers (diet specialists) but fewer species of searchers (diet generalists) can be "packed" along equivalent resource gradients (MacArthur and Levins 1967). Table 5 out- lines the set of predictions just summarized.

Measuring search/pursuit ratios

Although a number of authors use the terms searcher and pursuer, and several define them (MacArthur and Pianka 1966, Schoener 1969a, 1971), no one has attempted to do more than suggest what species belong to which category. We may intuitively assign search/pursuit ratios to particular species, but ulti-

mately we must make meaningful measurements in the field that confirm (or refute) what we intuit. Unfortu- nately, the measurement of simple budgets of time (or energy) spent in search and pursuit is not feasible in many situations. Before the success of modeled predictions can be examined, it is important to consider if and how actual species can be categorized as searchers or pursuers.

The major obstacle is to assign intent or purpose to a bird's behavior while measuring time passed or energy consumed. Pursuit is a directed form of behavior that in general can be readily identified. Searching behavior can also be identified fairly easily in birds that are highly active searchers (e.g., swallows), for when the bird stops actively searching (when the swallow ceases sweeping through the air), it is reasonable to conclude that it has stopped searching altogether. The matter becomes complicated, however, with birds that are only moderately active or passive searchers. A flycatcher, for example, sits on a perch, often for extended periods, watching and waiting for prey to enter its field of view. Is it reasonable to assume that the bird is always searching during the entire period? Could it not spend part of its time watching for rival males, keeping sight of its mate, resting, singing, or perhaps even allowing its attention to wander? We have no way of knowing, no way of assigning intent to behavior that is not visibly directed, and hence no way of determining how much of that behavior is actually spent in searching. This is a problem in any species that does not employ a continuous, active search behavior. Even relatively active warblers are often observed to pause for several seconds or more. Frequently they cock their heads and peer about, apparently taking a closer look at the neighborhood. But at other times, they stop to scratch, stretch, or preen. And sometimes, they simply stop. Are they still searching, or not?

The question may be unnecessary if, as some have suggested (Schoener 1969a), birds can maintain normal search behavior while simultaneously performing


TABLE 6. Mean attack radius in singing and nonsinging periods.

Mean attack radius (M + SE) Per-

cent Non- differ-

Species singing Singing ence*

Dusky Flycatcher 1.2 ? .1 3.6 ? .8 +211 Willow Flycatcher 2.0 ? .2 2.5 ? .4 +26 Western Flycatcher 2.1 ? .6 1.3 ? .2 -37 Western Wood Pewee 3.8 ? .2 6.0 ? .6 +58 Olive-sided Flycatcher 8.0 ? 1.0 20.6 ? 12.7 +158

* Calculated as singing - (nonsinging) x 100. nonsinging

other tasks, such as territorial defense. To test this, I took the foraging data for all eight species and com- pared what I have called singing and nonsinging data. Because singing data consists of all observations during which the bird sang, no matter how briefly, it includes a great deal of nonsinging foraging time as well. Therefore, singing data is a conservative estimate of foraging behavior during territorial defense (of which singing is used as the primary indicator).

Among the members of the fly-catching guild there is a trend in longer attack radii during singing periods (Table 6). (This is only a trend since statistical tests on the present data do not indicate significant differences.) The pattern suggests that when birds are at- tentive to the possibility of rival males at the periphery of their territories they also may be capable of searching for prey. As a result, prey are observed and attacked at longer distances than at times when the bird is simply foraging. While the implication here is that searching for rivals and searching for prey are com- patible behaviors at least in species with more passive pursuit modes, a variety of other data lead to the opposite conclusion. In all eight species, for example, velocity decreases during singing periods (Table 7). Birds apparently spend more time per perch during singing periods, implying that searching and singing cannot occur simultaneously. Similarly, foraging in-

TABLE 7. Velocity in singing and nonsinging periods. Veloc- ity is the total number of perches divided by the total number of minutes in all observations for each group of data. Percent difference calculated as in Table 6.

Velocity Per- cent

Non- differ- Species singing Singing ence

Wilson's Warbler 33.3 5.9 -82 Yellow Warbler 25.0 10.0 -60 Yellowthroat 10.0 3.6 -64

Western Flycatcher 3.8 2.7 -29 Willow Flycatcher 2.9 0.8 -72 Dusky Flycatcher 2.6 0.8 -70 Western Wood Pewee 2.2 0.9 -60 Olive-sided Flycatcher 0.6 0.5 -24

TABLE 8. Foraging intensity in singing and nonsinging periods. Foraging intensity is the total number of attacks divided by the total number of minutes in all observations for each group of data. Percent difference calculated as in Table 6.

Foraging intensity Per- cent


Yellow Warbler 4.65 1.59 -66 Wilson's Warbler 3.14 1.17 -63 Yellowthroat 1.74 .35 -80

Western Wood Pewee 1.78 .47 -74 Western Flycatcher 1.25 .58 -54 Dusky Flycatcher .95 .18 -81 Willow Flycatcher .84 .23 -73 Olive-sided Flycatcher .26 .16 -38

tensity decreases dramatically in all eight species during singing periods (Table 8). Thus the number of attacks per minute is considerably lower during periods of defensive behavior. In addition, the amount of time spent on dead perches increases during singing periods for seven of the eight species, and to a significant degree in four (Table 9).

The combination of foraging and singing must thus be considered a compromise. Although it is clearly advantageous energetically to forage (as time permits) while singing, the foraging thus performed is not as effective as during true foraging bouts. Velocity, and hence the area searched, decreases, the rate of attacks is lower, and greater time is spent in possibly less favorable foraging space (e.g., dead perches). In es- sence, territorial behavior requires time that could otherwise be used in search. As a result, I believe the assumption that territorial defense can be performed within the context of normal search behavior is inval- id. Indeed, any nonforaging behavior will probably compromise normal foraging patterns. Thus, for those species that perform some amount of passive search-

TABLE 9. Time spent on dead perches in singing and nonsinging periods. Figures are percent of total observation time for each group of data. Percent difference calculated as in Table 6.

Percent time Per- cent


Yellowthroat 20 63 +215** Wilson's Warbler 22 49 + 123** Yellow Warbler 22 24 +9

Olive-sided Flycatcher 56 49 -13 Western Flycatcher 82 90 +10 Dusky Flycatcher 86 97 + 13** Willow Flycatcher 88 96 +9 Western Wood Pewee 92 97 +5**

** Differences significant at the 1% level using the test of equality of two percentages (Sokal and Rohlf 1969:607).


ing, it is not safe to assume that all passive behavior is search behavior. Other types of behavior (defense, rest, etc.) may also be performed passively at the ex- pense of search time. Until it is possible to assign mo- tives to the different forms of passive behavior, all such passivity will remain indistinguishable in the field, and the measurement of time or energy expended in search will continue to be an elusive goal.

Even if there were a way to measure search/pursuit ratios, there are additional serious difficulties. Several authors have pointed out that there are different ways to optimize diet. Griffiths (1975) distinguishes two types of optimal foragers: one that feeds to maximize energy intake and one that feeds to maximize the number of prey taken. Schoener (1969b) and Pulliam (1974) consider a somewhat difference distinction: an optimal forager may be either an energy maximizer (to yield "the greatest net energy gain for a given time spent feeding" [Schoener 1969b]) or a time minimizer (to meet "its energy requirement in the least amount of feeding time" [Schoener 1969b]). Thus, even if it were possible to determine search and pursuit budgets, one would still have to establish the relevant units, energy, time, or numbers. As I have already noted, some model-builders do not distinguish between budgets measured in time or energy. It may not be necessary to decide whether the species under study are energy, time, or number optimizers, and hence what to measure, if the different budgets produce the same result. However, it is easy to imagine situations where different budgets give conflicting results. Passive searchers, for example, require little more than maintenance metabolism for search, while the amount of time spent is probably relatively large. Active searchers, however, must invest a large amount of energy in search, although the amount of time spent searching is often relatively small (Salt 1967). The resulting search/pursuit budgets would be significantly different in the above example, depending upon whether one measures time or energy. To make matters more complex, shifts in prey abundance could result in a shift from one optimization strategy to another (Griffiths 1975). In addition, a bird's strategy could shift during the course of the breeding cycle; an incubating female would likely be a time minimizer, but later, when feeding young, she might be an energy maximizer. (C. P. Black, personal communication). Nor is it at all clear that searchers and pursuers necessarily optimize the same thing. These problems make it impossible as yet to obtain meaningful measurements of search/pursuit ratios such as would be needed to identify objectively searchers and pursuers.

We now have a considerable body of theory concerning searching and pursuing predators but are un- able to measure the critical defining quality, the search/pursuit ratio. In contrast, we can relialy measure and define active and passive searchers, but these data have not yet generated a theoretical framework

upon which to hang our observations. Is there some relationship between these two spectra of predatory behavior that would allow us to join existing theory with measurable behavior? Schoener (1969a), in his definition of a Type I predator (pursuer), makes the assumption that such predators "passively locate" their prey and proposes flycatchers as an example. Schoener (1969a) also proposes warblers as an example of Type II predators (searchers). Common sense suggests as well that predators investing little or no energy in pursuit must actively seek out prey whose avoidance strategy is one of concealment rather than flight. In nature, it appears that species approaching the pure-searcher end of the spectrum are relatively active searchers (e.g., warblers, gnatcatchers, king- lets, titmice, vireos), while those species nearest the pure-pursuer end of the spectrum are relatively passive searchers (e.g., flycatchers, kingfishers, trogons). So long as it is impossible to measure the defining property of searchers and pursuers, the search/pursuit ratio, we can do little more than intuit that relationship. However, supported by my own opinions and those of others (e.g., Schoener [1969a]), I will for the remainder of the paper consider gleaners (as active searchers) to be searchers and flycatchers (as passive searchers) to be pursuers.

Gleaners and flycatchers as optimalforagers

How well do the results of this study fit the generalizations of Table 5? The first prediction holds that pursuers are diet specialists, while searchers are diet generalists. A possible indirect measure of specialization in food is the diversity of attack modes or attack substrates (Table 3, columns 1 and 2). The ranges of J exhibited by both guilds are wide and much alike, though the guild of flycatchers includes species of slightly greater generalization (higher J) than does that of gleaners, just the opposite of the prediction.

The second prediction states that searchers are habitat specialists while pursuers are habitat generalists. Habitat specialization can be estimated in at least three different ways. (1) There is no consistent pattern in either guild in terms of the degree to which territory vegetative composition differs from that of the habitat as a whole (Fig. 3). (2) Both guilds show a widely overlapping range of diversities (J) of vegetation types utilized in perching (Table 3, column 3). However, the range of values is considerably greater in the fly-catching guild, with the result that three species of flycatcher have J values greater than any warbler, i.e., they are more generalized, as predicted. (3) When evalu- ated by diversity of structural aspects of height and distance (what I have called foraging space), the results again confirm the predictions: in perch height, attack height, and attack distance (Table 3, columns 4-6), gleaners as a group are consistently more specialized (have lower J) than flycatchers.


TABLE 10. Overlap values for distance and height distributions in gleaners and flycatchers. Height overlaps are given to the upper right of the diagonal, distance overlaps to the lower left. See Methods for the formula used.

Olive- Dusky Willow Western Western sided

Wilson's Yellow Yellow- Fly- Fly- Fly- Wood Fly- Warbler Warbler throat catcher catcher catcher Pewee catcher

Wilson's Warbler X .85 .71 Yellow Warbler .96 X .63 Yellowthroat .95 .98 X Dusky Flycatcher X .89 .40 .64 .19 Willow Flycatcher .88 X .46 .68 .25 Western Flycatcher .82 .85 X .57 .32 Western Wood Pewee .54 .63 .54 X .20 Olive-sided Flycatcher .29 .38 .41 .65 X

The third generalization of Table 5 states that species of pursuers should have overlapping territories or show foraging sympatry, while species of searchers should have nonoverlapping territories or show foraging allopatry. Table 4 shows that the degree of territorial overlap with other individuals of the same guild is similar in both groups, though overlap is slightly less in the flycatchers. We can measure foraging sympatry or allopatry by the amount of overlap in foraging heights and distances (Table 10). Overlap in distance among warblers is quite high, ranging from .95 to .98. Among flycatchers, overlap is generally much lower, ranging from .29 to .88. Overlap in height distributions shows a similar pattern, although there is some overlap in the range of values between the two guilds. Gleaners, then, overlap extensively in both foraging height and distance with other gleaners, while flycatchers, more variable in both their height and distance distributions, overlap less with other flycatcher species. Thus neither part of the third prediction is supported.

The fourth generalization of Table 5 predicts that searchers will be similar in body size, while pursuers will have distinctly different body sizes. Body size is often measured by weight or wing length (Fig. 1); by both indicators, all the members of both guilds are significantly different (P < .02 or better [extended Tukey procedure; Spj0tvoll and Stoline 1973]), with the exception of the Western Flycatcher. However, statistically significant morphological differences do not necessarily imply ecologically significant differences. Schoener (1965) has defined small (i.e., not ecologically significant) differences as those in which the ratio of the larger to the smaller is < 1.14 in comparisons of bill size or wing length (used as a measure of body size). Ecologically significant differences generally have ratios > 1.14. Exclusive of the Western Flycatcher, difference ratios for weight, wing length, and bill length and width are given in Table 11. Wing length and weight ratios invite the same interpretation: gleaners are not ecologically different from one another, while flycatchers often are (with the exception of the two Empidonax). Bill width

parallel the pattern for weight and wing length, while both guilds show varying degrees of difference in bill length. Thus measures of body size vary in their agree- ment with the predictions.

Although Table 5 (number 5) predicts that sexual dimorphism should be prevalent among pursuers and lacking in searchers, the extent of dimorphism is essentially the same in the two guilds (Table 2). Finally, it is predicted that more species of pursuers than of searchers can be "packed" along certain equivalent resource gradients (Table 5, number 6). Of what I have called full guild members, there are four flycatchers and three warblers. Although these numbers appear to support the prediction, one should be aware that they are strongly dependent upon the size of area under study, the precise definition of sympatry employed in such local situations (i.e., other workers with other definitions could easily have decided upon 3 flycatchers and 3 warblers, or 3 and 2, instead of 4 and 3), and the necessarily arbitrary way in which species are included in or excluded from local guilds. In addition, it is not clear that the resource states of the two guilds are here "equivalent." This last prediction, then, is particularly difficult to test, and the data from this study are not entirely sufficient for that task.

As exemplified by my data for these eight species of birds, the fit between reality and theory is poor. Although it is difficult to assign cause for this to any single factor, there are a number of possible problems that may be working in concert to decrease the success of the predictions. One possibility is that theoretical frameworks such as these may, in fact, describe broad geographic patterns better than local circumstances. Karr and James (1975), for example, in studying a large number of Old World warblers (Sylviidae) and flycatchers (Muscicapidae), concluded that warblers are generally similar in foraging behavior and morphology, and segregate mainly by habitat, while flycatchers are more alike in the wide variety of habitats utilized and segregate primarily by means of foraging patterns and morphology. These findings agree with the substance of the first four generalizations of Table 5 in terms of geographic, rather than local patterns. It


TABLE 11. Difference ratios for four morphological characteristics in gleaners and flycatchers. Given in ascending size sequence, ratios of larger to smaller.

Wing Bill Bill Guild Species Weight length length width

Gleaners Wilson's Warbler 1.09 1.04 1.20 1.01 Yellow Warbler 1.09 1.09 1.04 1.01 Yellowthroat

Flycatchers Dusky Flycatcher 1.06 1.03 1.12 1.17 Willow Flycatcher 1.06 1.03 1.12 1.17 Western Wood Pewee 2.20 1.24 1.40 1.33 Olive-sided Flycatcher

should be noted, however, that Karr and James (1975) support their results more with a broad knowledge of natural history than with any extensive quantitative study. Second, it is possible that many generalizations apply only to specific situations that may or may not be explicit in the model. Schoener (1969a), for example, predicts a predominance of sexual dimorphism in pursuers, and further points out that insectivorous species inhabiting tropical seasonal forests should show dimorphism especially well, while those inhabiting temperate deciduous or conifer forests should exhibit it only rarely. The results of the present study lend support to Schoener's (1969a) qualification.

Another possible problem is that optimization may be static (essentially short term) or dynamic (long term) (Katz 1974). The outcomes of these two different strategies need not be the same (Krebs 1973). Thus, while we may fail to confirm an optimal strategy of one type (even though we may not be specific about which one we are dealing with), this need not rule out optimal strategies of another type. A fourth possible difficulty is that the extreme forms of behavior (e.g., pure searchers and pure pursuers) chosen as possible limits of response are probably not at all realistic, but are merely useful simplifiers to aid in the construction of the model. The extremes found in nature may actually be rather far from the extremes of the model spectrum; thus the actual response to a situation being tested may be less clear-cut than the model would have us expect.

A final problem may be that the models fail to take into consideration the strength of interactions among species that lie at the extremes of (or otherwise clumped along) the predatory spectrum, i.e., the interactions within guilds. It is quite possible that the internal organization of each guild, created by the forces of competition, overshadows the patterns modeled across guilds. If this is the case, it may be more profitable to approach optimal foraging from the point of view of adaptive syndromes, to compare the interactions within groups of species with similar syndromes, rather than to study the interactions among species exhibiting widely different adaptive syndromes.

Adaptive syndromes: An alternative approach

If we can isolate a limited number of distinct adaptive syndromes in insectivorous birds (and by extension, in predatory species in general), then it should be possible to predict a wide range of characteristics of a predator's lifestyle simply by determining which adaptive syndrome best describes its behavior. I suggest that there is a small set of adaptations, "core adaptations," that is basic to and identifies each adaptive syndrome. The complete set of characteristics displayed by the adaptive syndrome of a species results from an accumulation of optimal adaptive responses by other aspects of the species' biology to these few core adaptations. A species, then, could be identified by the core adaptations it displays, and a knowledge of these core adaptations should suffice for an accurate prediction of the species' entire adaptive syndrome.

In the evolution of a species, core adaptations are major changes, probably acquired before the numerous other adaptations that we now collectively view as the species' lifestyle. These many other characteristics are a response to one or more core adaptations as well as to environmental exigencies. Limitations imposed by different morphologies, restrictions placed by competition for resources, and the response to somewhat different environmental circumstances result in evolution of the slight differences we detect between members of the same guild. It is the evolutionary response to the same core adaptations that results in overall similarity among members of a single guild that share one adaptive syndrome.

Two adaptive syndromes in insectivorous birds have been identified in the course of this study. I have given them names that I feel exemplify their core adaptations: active searchers and passive searchers. Species exhibiting these adaptive syndromes can be distinguished readily by the attack modes they employ, their velocity, and their search intensity; I have already suggested a number of other bird groups that appear to exhibit the core adaptations of these two syndromes.

If we look for these identifying characteristics in


TABLE 12. An outline of the adaptive syndromes of active and passive searchers.

Active searchers Passive searchers Comparable in some ways to what have been called Comparable in some ways to what have

searchers or widely-foraging predators (Pianka been called pursuers or sit-and-wait 1971). predators (Pianka 1971).

CORE ADAPTATIONS 1. Foraging repertoire associated with passive prey, 1. Foraging repertoire associated with

which are hard to find, easy to catch. active prey, which are easy to find, hard to catch.

2. High velocity (perches/minute). 2. Low velocity. 3. High search intensity (perches/attack). 3. Low search intensity.

OTHER ADAPTATIONS 4. High foraging intensity (attacks/minute). 4. Low foraging intensity. 5. Small attack radius. 5. Large attack radius. 6. Small foraging space (structural diversity of 6. Large foraging space.

foraging microhabitat). 7. Species usually differ in critical morphological 7. Species usually differ in critical

dimensions (wing, weight, bill) by ratios <1.14. mrophological dimensions (wing, weight, bill) by ratios >1.14.

groups other than birds (with modifications for the specific behavior of particular taxa), many different animals appear to have evolved one or the other of these two adaptive syndromes. Pianka (1966, 1971), for example, distinguishes two methods by which car- nivorous lizards capture their prey. He calls one type a sit-and-wait predator: it waits passively "until a moving prey item offers itself," and then pursues it (either by chase or ambush). Pianka (1971) includes the iguanid lizards of North America, the agamids of Australia and the agamids and certain lacertids of Af- rica as sit-and-wait predators. He refers to the other type of lizard predator as "widely-foraging," and as the name implies, it moves actively through the habitat, searching for prey. The teid lizards of North America (Cnemidophorus), the skinks and varanids of Australia, and the skinks and certain lacertids of Af- rica are included in this second group. Many species of coral reef fishes actively and visually search for small cryptic crustaceans and numerous other invertebrates hidden in the reef (Bakus 1966, Ehrlich 1975), including many Labridae, Chaetodontidae, Muraoni- dae, and Brotulidae (Hobson 1974, 1975). Other species of fishes, often cryptically colored, sit and wait for unwary prey, and ambush them with a quick dash (including many Synodontidae, Scorpaenidae, Bothi- dae, and Cirrhitidae [Hobson 1974, 1975]). There are also examples of active and passive searchers among invertebrates. Turnbull (1973) notes that many genera of the spider family Thomisidae ambush prey after waiting motionless for their approach. Other families of spiders (Salticidae, Lycosidae, Pisauridae) have powerful eyesight and are classified by Turnbull (1973) as more active searchers. Many other taxa exhibit the characteristics of these two adaptive syndromes.

It is likely, then, that the basic identifying charac-

teristics of active and passive searchers are widespread among predators in general. In light of this, it would be useful to describe here an outline of the two adaptive syndromes and to apply the results of this study of gleaners and flycatchers to generalizations about predators of many different types. In proposing such generalizations, I am at the same time suggesting a direction of inquiry that may prove fruitful for increased understanding of predation. Clearly, many predators of different taxa should be studied to test the universality of these two adaptive syndromes, and to identify the numerous other predatory syndromes that undoubtedly exist.

A general outline of the adaptive syndromes of active and passive searchers is presented in Table 12. All of the characteristics included are measurable in the field (with some modification, of course, for groups whose foraging behavior differs from insectivorous birds due to different morphology, habitat, prey, etc.) and should apply to local situations as well as broad geographic areas. In the first part of Table 12 I have indicated a general correspondence between active searchers and such terms as (pure) searchers and widely-foraging predators, and passive searchers and (pure) pursuers and sit-and-wait predators. However, it is important to point out that this is merely a general correspondence; the synthesis presented here is an attempt to alleviate difficulties that have accompanied use of these other terms, and is not simply an addition of new names to existing concepts.

I join several other authors (Cody 1973, Hespen- heide 1975a) who hold the opinion that the way a predator catches its prey is one of the most important characteristics of that species' natural history. It may well be the single most important characteristic. For this reason, I have listed as the first core adaptation the


foraging repertoire, which is a product of preferred prey and their ease of capture (Table 12). Taxa other than the birds studied here may employ somewhat different attack methods (ambush, stalk, dive, run, etc.) but the distinction between the two syndromes should be basically the same. I have included two other characteristics as core adaptations, velocity and search intensity, since, together with foraging repertoire, they provide the clearest picture of the differences between the two groups. In addition, the three characteristics together are the most reliable defining qualities for the two syndromes. They also appear to have the greatest potential for isolation and description of other adaptive syndromes. Additional studies may suggest that foraging repertoire is the sole characteristic worthy of description as a core adaptation, or that there are many core adaptations. Assignments such as this are necessarily subjective at this point and perhaps always will be.

The remainder of Table 12 (lines 4-7) lists additional characteristics that reflect other areas of contrast between active and passive searchers including behavior, utilization of space, and morphology. Other comparisons are, no doubt, possible, as are perhaps more detailed elaborations on the generalizations presented here. Such elaborations are, however, contingent upon further studies of ecologically closely related groups such as sweepers (swallows and swifts) and vireos, as well as comparative studies of active and passive searchers in other taxa, such as lizards and reef fishes.

This paper considers predation from the point of view of adaptive syndromes, comparing two guilds of predators in order to describe and distinguish the characteristics of their syndromes. I have used this method of analysis because I believe the relationships between the adaptive syndromes of different species and guilds most clearly describe the organization and structure of the community of which they are a part. If, as I have suggested, groups of predators can be isolated and classified by adaptive syndromes, much as has been done for insect herbivores (e.g., Root 1973, 1975), then further study on the community level will serve to identify the different syndromes, describe their attributes, and determine the actual species characterized by each. Far from destroying the elaborate structure offered by present optimal foraging models, the adaptive syndrome approach can help to reconstruct the theory to better reflect the discoveries of field workers, both by pointing out its shortcomings, limitations, and errors and by identifying the correct assumptions and predictions. As data on a variety of species and their adaptive syndromes accumulate, it will eventu- ally be possible, through the approach used here, to generate predictions complementary in nature and scope to those currently provided by optimal foraging theory. Further work from both points of view, optimal foraging and adaptive syndromes, will surely in-

crease our understanding of the patterns of predation in nature.

ACKNOWLEDGMENTS

This paper is based on a dissertation submitted in partial fulfillment of the requirements for the Ph.D. to the Section of Ecology and Systematics, Cornell University. I owe special thanks to those who assisted me in the field: L. Vaughan, P. Nelson, K. Rosenberg, T. Bailey, and R. Bonney. I am also especially grateful to the many people in Rocky Moun- tain National Park, particularly R. Haines, who made it possible for me to work in the park and helped me in countless other ways. I am indebted to S. Fretwell, who planted the seed of the idea that grew into this research, although he may not recognize it after a number of years of change. R. B. Root provided constant encouragement, advice, and support throughout the duration of the project. In addition, the members of the Comparative Ecology Guild at Cornell have been a constant source of ideas and useful criticism. P. Hyypio of the Bailey Hortorium at Cornell kindly identified the sedges and shrubs of the study area. R. B. Root, W. L. Brown, Jr., P. L. Marks, R. H. Whittaker, P. McEvoy, C. P. Black, and an anonymous reviewer offered valuable suggestions and comments on the manuscript.

The curators of the following collections graciously al- lowed me to inspect and measure their specimens of warblers and flycatchers: the Denver Museum of Natural History; the Zoological Collections, University of Colorado Museum; the Department of Zoology and Entomology, Colorado State University; the National Fish and Wildlife Laboratories, U.S. Fish and Wildlife Service, Fort Collins, Colorado; the Natural History Collections, Rocky Mountain National Park; the Department of Ornithology, American Museum of Nat- ural History; the Museum of Comparative Zoology, Harvard University; and the Vertebrate Collections, Cornell Univer- sity.

This research was made possible with the generous finan- cial support of the following: the Cornell Research Grants Committee; the Graduate School of Cornell University; the Section of Ecology and Systematics, Cornell; the Du Pont Educational Fund of the Section of Ecology and Systematics, Cornell; the Cornell Chapter of the Society of the Sigma Xi; the Louis Agassiz Fuertes Research Fund of the Wilson Or- nithological Society; and the Frank M. Chapman Memorial Fund of the American Museum of Natural History. The De- partment of Zoology, University of Maine at Orono, paid page charges.

Finally, I must thank one who wishes to remain anonymous for unfailing assistance, encouragement, and support.

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the adaptive syndromes of two guilds of insectivorous birds in the colorado rocky mountains

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