Studies in Avian Biology No. 13:144-160,

1990.

A CLASSIFICATIONSCHEME FOR FORAGING
BIRDS IN TERRESTRIAL
HABITATSJ.V.

BEHAVIOROF

REMSEN,JR. AND SCOTT KROBINSON
Abstract. Studiesofavian foragingbehavior in terrestrialhabitats sufferfrom a lack of standardizationin the kinds of data gatheredand in the terminology used to classifydifferent activities. These inconsistenciespartially reflect the variety of questionsaskedabout foraging.If a standardterminology wereused, then data on foraging behavior could be included among the standard data (e.g., clutch size,
body weight, and mating system) routinely recorded for the biology of a bird species.
We propose a system for gathering foraging data for landbirds in which the five basic, sequential
componentsofforaging (search,attack, foragingsite, food, and food handling) are quantified separately.
Data on searchingbehavior involve measuringcontinuous variables and are particularly critical forstudies of energetics. The “attack” component is most in need of standardized terminology. The
systemthat we propose separatesthe attack perch from the attack maneuver, and further subdivides
the maneuvers into near-perch, subsurface,and aerial maneuvers. Each of these general categoriesis
further subdivided accordingto details of attack movements and ways in which substratesare manipulated. Data on attack methods are primarily useful for studies of ecomorphology, but may also
be important in bioenergeticand community-level studies.
Quantifying the foraging site involves measuringthe following variables: general habitat (location
in a study area), vertical position, foliage density, and substrate.Although identification and quantification of foods taken in the field is difficult, it can provide valuable information on food size (andtaxon for largeritems). Dietary data from stomachsamplesare usefulfor studiesof resourcepartitioning
when they show dramatic differences,but overlapping diets do not necessarilyindicate that two birds
forage in the same way. Food-handling behavior is seldom measured in the field, but is valuable instudiesof optimal foraging behavior and ecomorphology.
Intercorrelationsbetween each of these aspectsof foragingcan be determined from standardmultivariate analyses.How finely to subdivide categoriesdependsupon the kinds of questionsbeing asked.
Foraging behavior classification;foraging maneuvers; search;attack; foraging site; diet;food-handling; glean; sally; probe; manipulate.

Key Words:

There are almost as many ways of classifying
and quantifying foraging behavior as there are
papers on the subject. In part, this variety reflects
the fact that no two species or groups of species
forage in exactly the same way, and that no two
habitats present exactly the same foraging opportunities. It is difficult, for example, to quantify the foraging methods of bark-foragers in thesame way that one quantifies the foraging of foliage-foragers (Jackson 1979). Another factor
contributing to the lack of standardization is thatdifferent kinds of questions often require different kinds of data. Many studies that focus on
resource partitioning record only the details of
foraging site selection and omit data on search
and attack movements (e.g., Hertz et al. 1976).
In contrast, studies of ecomorphology emphasize
prey-attack methods (e.g., Osterhaus 1962; Fitzpatrick 1980, 1985) whereas bioenergetic andoptimal foraging studies emphasize searching
movements as well as prey handling (e.g., Sherry
and McDade 1982, Robinson 1986). Even studies addressing the same questions in ecologicallysimilar birds do not always measure the same
variables.
This lack of standardization, however, reflects
fundamental inconsistencies in the importanceattached to the individual variables used toquantify foraging. For example, the “hawk” category of Sherry (1979) and Holmes et al. (1978,
1979b) includes attacks on prey animals that were
flying when first seen, attacks on prey flushedfrom foliage by the foraging activities of the bird,
and chases after prey that the bird attacked andmissed. Later papers by Robinson and Holmes(1982, 1984) and Sherry (1983, 1984) however,showed that differences among these aerial maneuvers have important implications for diet.
Remsen (1985) showed that the fine details of
substrate use (e.g., dead leaves, moss) that areoften ignored in many community studies wereparticularly important in resource partitioning ina tropical bird community. Rosenberg (this volume) further showed that even within a group as
specialized as dead-leaf foragers, speciesdiffer inthe kinds of suspended dead leaves that they
search. The classification of foraging behavior,
therefore, is more than a semantic problem: one
can reach different conclusions simply by classifying foraging methods differently.
In this paper, we propose a system for measuring and classifying foraging behavior for nonraptorial landbirds. Our goal is to standardize
data-gathering methods and terminology to permit among-site and among-species comparisonsthat are currently handicapped by the absence of144

CLASSIFICATION

OF BEHAVIOR--Remsen

a common vocabulary. If some standard systemand terminology were used by those studying
foraging behavior, then we could ask questions
concerning the frequencies of various behaviors
among communities. Such comparisons may
provide important insights into community organization: in a field such as foraging behavior,in which community-wide experimental manipulations are difficult or limited, a comparative
approach among species and communities may
be the only method available for testing many
hypotheses.
The system presented here separates five sequential components of foraging behavior, eachof which is quantified separately when data aregathered in the field: (1) search (movements leading up to sighting of food or food-concealing substrates); (2) attack (movements directed at food
item or the substrate that conceals it once sighted); (3) foraging site (including general locationand specific substrate); (4) food (including typeand size); and (5) food handling (after food item
obtained). We recognize that many of these components are not necessarily independent, but we
prefer to quantify each separately and to allow
subsequent analyses to show intercorrelations.
At the outset, we recognize that any classification system inflicts typology on what may be
gradients of behavior, but we see no other practical solution for organizing foraging information. Our goal is to distinguish among what we
subjectively perceive to be functionally different
categories. By using standardized terminology,
data on foraging behavior can be included among
the standard biological data reported for bird
species. At present, reference works on birds,
which typically include detailed, quantitative dataon variables such as clutch size, body weight,
molt and migration schedule, and mating system, tend to omit, or describe in superficial, qualitative ways, all aspects of foraging behavior except perhaps diet. Foraging data should be
included in such reference works, because foraging behavior is an integral part of a species’
biology, and becauseit relatesto time-activity budgets, morphology, habitat selection, and social
system. The foraging behavior of many species
may also be as “typical” of that species as anyother aspect of its biology. A standard vocabulary will eventually allow a more sophisticatedreview of the prevalence of various foraging behaviors in birds; such a review will be able toreplace the often anecdotal, “who-does-what”
approach with quantitative comparisons between taxa and regions.
The heart of this paper is the section on theattack, which is the phase of foraging that is mostin need of a standard terminology based on functionally different categories (cf. Moermond, thisand Robinson

145

volume). We discuss briefly data on bird diets,
and also propose a standard terminology for foodhandling techniques. The final section of our paper deals with some of the ways in which data
can be analyzed to address questions of resourcepartitioning, bioenergetics, and ecomorphology.
SEARCHING

BEHAVIOR

Searching behavior includes those movements used
to search for food or substrates that hide food; under
our definition of searching behavior, “search” ends
once food or food-hiding substrates are sighted andattacked. Searching methods have usually been quantified by recording the lengths and rates of movements
between perches and the time intervals between movements (e.g., MacArthur 1958, Cody 1968, Williamson
197 1, Fitzpatrick 198 1, Robinson and Holmes 1982).
Other variables are: (1) distance covered per unit time;(2) number of stops and time-spent-stopped per unit
time; (3) number of attacks (and % successful) per unit
time; (4) direction ofmovement between stops, in three
dimensions if appropriate; (5) sequential distributionof locations of stops (to calculate return rates to previous stops). Between-foraging-site movements can be
categorized as: (1) walk, (2) hop, (3) jump (leg-powered
leaps that cover more space than the typical hop), (4)run, (5) climb (with notations on whether or not the
tail is used as a brace), (6) glide, (7) flutter, and (8) fly.
Robinson and Holmes (1984) further distinguished between hops in which American Redstarts (Setophagu
ruticilla) fanned their tails and lowered their wings,
and hops in which there were no extra movements.
Some birds also use their wings for support when hopping on thin, weak perches, a movement that could becalled a “flutter-hop” (Robinson, unpubl. data). Alsoof interest are postures during searching that are seldom qualitatively described (for exceptions, see any E.
0. Willis reference) or quantified but that may havesubtle morphological correlates. Postures are particularly difficult to categorize because most species moveand change postures frequently, and because head, wing,
and tail orientations are all simultaneously involved.
Perhaps the advent of telephoto video-cameras will
permit such analyses; in this paper we deal with postures only peripherally. More amenable to quantification are changes of orientation while searching froma perch, either with head or body movements. For
example, many species have characteristic side-to-side
movements, whereas others maintain a straight-ahead
orientation. Many species have characteristic wingflicking or tail-wagging movements that accompany
foraging, the significance of which is not often understood: the frequency of such actions could also be quantified.‘There is alsoa parallel literature on the searching
behavior of various lizards (Moermond 1979, Huey
and Pianka 1981).
In general, searching movements of birds form acontinuum from “active” to “passive” modes (Eckhardt 1979). Active foragers change perches at a highrate, including many hops (or steps in species that walk),
and most flights are short. Passive foragers seldomchange perches, but fly long distances when they do
move. The subset of birds that Eckhardt (1979) chosefrom the community that he studied fit into active

146

STUDIESIN AVIAN(primarily wood-warblers) and passive (primarily tyrannids) foragers. A subsequentstudy of a different
forest bird community (Robinson and Holmes 1982)
however, found that many speciesdid not fit cleanly
into either category.Tanagersand vireos, for example,
were intermediate in their rates of hopping and flying
and in the lengthsof their flights. Another species,theAmerican Redstart appearedto add many movementsof its wingsand tail designedto flush prey to its alreadyactive foraging behavior. Furthermore, the searching
movements ofthe Black-cappedChickadee(Puntsatricapillus)depended upon the distribution of whatever
substrate(e.g.,dead leaves)an individual of this species
wassearchingat the time. Searchingmovements, therefore, cannot necessarilybe categorizedtypologicallyin
the same way as attack maneuvers (see below). We
agreewith the approachof most authors who quantify
and present data on searchingmovements separately(e.g., Robinson and Holmes 1982, Landres and
MacMahon 1983, Holmes and Recher 1986b).
Many birds use food-searching methods that are
similar to attackmethods(seebelow). Robinson(1986),
for example,quantifiedthe rate at which Yellow-rumped
Caciques(Cucicusda) used the following searchtactics:“probe-searches,”in which an individual searcheda dense cluster of leaves; “hover-searches,” in which
an individual searchedthe tips of foliage while hovering under them in stationary flight; and “hangsearches,” in which an individual searcheda nearby
substrate while suspendedbelow it. If any of thesesearchingtactics led to a prey capture, then they were
quantified separately as prey attack maneuvers. The
only differencebetweena “probe-search”and a “probeattack” (see below) was in whether or not prey was
located. This illustrates a problem in distinguishing
between searchingand attack methods in speciesthat
search for concealed food: any classification system
inevitably includesdata on both searchingand attacking behavior. Woodpeckers,for example, both search
for and attack prey by removing an outer layer of bark.
We have chosen to classify these methods as attacks(seebelow) on food-concealingsubstrates.Distinguishing between search and attack phases,however, representsan unresolved issuein some parts of our classification scheme,especiallyfor those speciesthat peer
closelyand unambiguouslyat particularsubstrates,suchascurled leaves,leaf tops, and crevices.Although these
speciessearcha particular substratein a manner thatis analogousto any of the substrate-manipulationmaneuvers outlined in the attack maneuver section (seebelow), our scheme does not include “peering” or“scanning” as an attack maneuver. In the field, werecordsubstratesthat are unambiguouslysearchedwith
the notation “visual search,” but we are uncertain as
to how to include suchdata in analyses.Certainly, suchvisual searchesare important in analysesof substrateuse.
Severalother kinds of searchbehavior are sufficiently distinct to warrant separatetreatment. Many birds
follow disturbancesthat exposeprey; suchdisturbances
include fires, other animals (particularly other bird
species,ungulates,monkeys, and army ants), and humans and their machines. Many recent studies place
disturbance-followersin a separate guild (e.g., Karr
1980, Terborgh 1980a, Terborgh and Robinson 1986).

BIOLOGY

NO. 13Many birds steal food from other birds, and somespeciesrely on this tactic (kleptoparasitism)for locating
and capturingfood (seeBrockman and Barnard [ 19791
for review). Finally, some landbirds form mutualistic
food-searching associations
either with conspecifics(e.g.,
Kilham 1979, Mindell and Black 1984) or other bird
species(Jackson1985), especiallywithin mixed-species
flocks (e.g., Munn 1986). These sorts of associations
should always be recorded.
ATTACK BEHAVIOR
We define the “attack” phaseas that portion of foraging behavior from the moment when a food item,or food-concealingsubstrate,is sightedto the moment
when a capture attempt is made. Thus, we include
within “attack” phase those behaviors aimed at dislodging or revealing food before it is sighted, such as
various kinds of substratemanipulation (e.g., flaking,hammering, gaping). We further subdivide the attack
phase into (1) perch and (2) maneuver.
Few studieshave quantified parameters concerning
the characteristicsof the perch from which an attackis launched.The numerousstudiesby E. 0. Willis (seereferences)have shown that a species’presence in aparticular habitat or microhabitat may be determinedin part by availability of suitableperches.Certain species
may also specialize on perch types not used by otherspecies.For example, two small tanagers(Hemispingus
xanthophthalmusand H. verticalis)that characteristically searchthe uppersidesof leaves in dense clusters
do so by perching on the clustersthemselves (Parker
and O’Neill 1980; Parker et al. 1980, 1985). Several
speciesin the vireonid genus Hylophilus characteristically graspthe margins of leaves for perchesto reachthe undersidesof these leaves (T. A. Parker and JVR,
unpubl. data). Furthermore, studies such as those byPartridge (1976a; cf. Leisler and Winkler 1985) haverevealed important morphological adaptations associated with particular perch types.
Perchtype can be quantified usingthe samevariables
asthoseusedin our schemefor “substrate” (seebelow).
In practice,most measurementstaken for the substrate
will be the same as those for the perch except for thedetails of perch angle and diameter; therefore, the increasein volume of data to be recorded in the field isminimal. Those speciesthat search while moving do
not really have a “perch” per se; for instance, somespecies search and attack while in continuous flight(“screening,” seebelow) or while hovering (e.g., Say’s
Phoebe [Suyornis suyu], Grinnell and Miller 1944;
bluebirds [Sialia spp.], Power 1980; and RestlessFlycatcher [Myiagru inquieta], Ford et al. 1986).
Our classification of attack maneuvers categorizes
them with respectto the complexity and required agility of each behavior. For example, we assume thataerial maneuvers and substratemanipulation require
greater agility and more energy than those maneuvers
in which a food item is removed from a substratenext
to the bird’s perch. Our classificationalso attempts toremove where possiblethe influence of substrate;thus,
foraging motions that appear similar, but are directed
at different substrates,are groupedtogether.Such similarities may be superficial, and foraging motions arecertainly influencedby the types of substratesat which
they are directed. Nevertheless,we prefer to group to-CLASSIFICATION

OF BEHAVIOR--Retmen

TABLE 1. PROFQSEDCLASSIFICATIONSCHEMEFORATTACK METHODSOF THE FORAGINGBEHAVIOROF
NON-RAPTORIALLANDBIRDS, WITH SYNONYMSORPRESUMEDSYNONYMS
FROMOTHERSTUDIES(SEETEXT)
I. Near-uerch maneuvers
A. Surface maneuvers
1. Glean (= pluck, perch-glean, pick)
2. Reach (= stretch)a. Reach-up (= crane)
b. Reach-out
c. Reach-down (= lean, duck-under)
3. Hang (= hang-glean)a. Hang-up (= hang vertical, hanghead-up, vertical clinging)b. Hang-down (= hang head-down)c. Hang-sideways(= hang-side,
vertical clinging)d. Hang-upsidedown (= hanghorizontal)
4. Lunge (= dart, rush)
B. Subsurfacemaneuvers: no substrate
manipulation
1. Probe
C. Subsurfacemaneuvers:substrate
manipulation
1. Gape
2. Peck (= tap)
3. Hammer (= drill)
4. Chisel
5. Flake (= bill-sweep, toss)
6. Pry7. Pull
8. Scratch
II. Aerial maneuvers
A. Leg-powered maneuvers
1. Leap (= jump-glean, jump). Include
leap-distanceand leap-angle.
B. Wing-powered maneuvers
1. Sally (= hawk, snatch, flycatch,hover-glean, hover). Include
sallv-distanceand sallv-anale.
a. Sally-strike (= outward-strike,upward strike, snatch)b. Sally-glide
C. Sally-stall (= hover, hoverglean)d. Sally-hover (= hover, hoverglean)e. Sally-pounce (= land-and-glean,
pounce, dive-glean)
2. Flutter-chase
3. Flush-pursue
4. Screen(= hawk)

gether similar-appearing behaviors to alert morphologiststo these potential similarities, rather than to allow the substrate category to separate automaticallysuchbehaviors. Becausethe systempresentedhere also
requires that the substratealso be recorded, no information is lost by excludingsubstratesfrom the behavior categories.

and Robinson

147

In general, studies of attack behavior in landbirds
have distinguishedthe conspicuousaerial maneuvers
from other attack behaviors, but the nonaerial attack
maneuvers have often been lumped in one category,
usually“glean.” Suchmerging of nonaerial maneuvers
into one or a few categoriesmight obscureimportantbehavioral differencesamong speciesthat have implications for adaptive morphology (e.g., Richards andBock 1973, Partridge 1976a,Leisler and Winkler 1985),
searchtactics, niche overlap, and food selection.
Our classification(Table 1) does not include certain
maneuvers that appear to be rare, such as digging inground by using a strongly curved bill in a hoe-likemotion (Engels 1940) using spines and twigs as tools
for probing (reviewed by Boswall 1977), usingthe headas a brace to provide leverage for foot scraping(DeBenedictis 1966, Kushlan 1983) or as a buttressto
move or dislodgesubstrate(Keast 1968), vibrating feetto startleprey in leaf-litter (Hobbs 1954, Wall 1982 ascited by Edington 1983), rustling leaf-litter to startle
prey (Potter and Davis 1974), and crushingtwigs withthe bill to exposeprey therein (Mountainspring 1987).
The system in Table 1 can be expanded as needed toinclude any such rare behaviors.
Many studiesof foraging behavior that make interspecific comparisons, or intraspecific comparisonsamong seasonsor habitats, have presented their datain the form of a diversity index and have not included
the original data with percentageof observations ineach foraging category. Other studies have identified
the number of speciesin a community associatedwith
variousforagingcategories,but have neglectedto identify which speciesbelong in each category. We thinkthat the original data themselves should be presented
to facilitatecomparisonswith other studies;they shouldat least be published as appendices.
An outline of the categorieswith definitions of eachattack behavior follows. Some categoriesare not mutually exclusive. For example, a bird that “sally-hovers” might also “probe” while hovering. Therefore,
many attack maneuvers can have compound names,such as “sally-hover-probe” or “reach-out-gape.”
Each maneuver category is accompanied by someexamples from the literature. Our literature survey isintended to be illustrative rather than encyclopedic.
We tend to cite examples from recent, quantitative
studies, rather than older, more qualitative material.
Although the descriptivesectionsof the latter are often
superior,much of the older material is containedwithin more general life-history studies and is therefore
more difficult to locate.
In choosing a standard vocabulary, we have attempted to use simple, descriptive terms, which, if
possible,are already frequently used in studiesof foragingbehavior; we have not hesitatedto “synonymize”
many favorite terms, including many of our own.
I. Near-perch maneuvers (target food item can bereached from bird’s perch)
A. Surfacemaneuvers
1. Glean: to pick food items from a nearby
substrate,including the ground, that can bereachedwithout full extensionof legsor neck,no acrobaticmovements are involved. Emlen’s (1977) and Mountainspring’s (1987)

148

STUDIESIN AVIAN“pluck,” Fitzpatrick’s (1980) “perch-glean,”and Moermond and Denslow’s (1985) andRemsen’s (1985) “pick” are synonyms. Perhaps the majority of maneuvers performedby most foliage- and ground-searching birds
are “gleans.” For example, 5 1% of the forest
species studied in the Andes by Remsen(1985) and 53% of the forest species studiedin Australia by Ford et al. (1986) used glean
as their principal foraging maneuver. Because gleaning is presumably the least costly
maneuver in terms of energy expenditure,
it is not surprising that it is used so frequently (Remsen 1985; Moermond, thisvolume).
2. Reach: to extend completely the legs or neckupwards, outwards, or downwards to reachfood (after Moermond and Denslow 1985,
Remsen 1985). Because most studies seldom distinguish “glean” from “reach,” thefrequency with which “reach” maneuvers
are used is not generally known. Strong interspecific differences among congeners inability to reach are associated with morphological differences (Snow and Snow 197 1,
Moermond and Denslow 1985). Some frugivores, especially toucans and some tanagers, obtain their food by reaching (Moermond and Denslow 1985). Morse (1967b).
who distinguished “stretching”-whichisprobably equivalent to our “reaching”from gleaning, found that it was used seldomly (O-5% of all maneuvers) in the six
species of wood-warblers studied. Threefurther subdivisions may be made with respect to direction:
Reach-up:to reach above the bird. Thisis synonymous with the “crane”
ofGreenberg (1987b). This maneuver isused especially frequently to pick preyfrom undersides of leaves. The Palelegged Warbler (Basileuterussign&us)
uses this motion, along with the next,
more frequently than any other maneuver (Remsen 1985).
Reach-out:to reach lateral to the bird. A
maneuver used especially frequently topick prey from nearby leaves andbranches.
Reach-down:to reach below the plane of
the feet. This is synonymous with the“lean” of Greenberg (1987b) and probablv the “duckina-under”
of Rabenold(1980). This man&ver is used by manytanagers, especially Tanguru, when foraging on branches (Snow and Snow 197 1;
Skutch 1981; Parker and Parker 1982;
Remsen 1984, 1985; Hilty and Brown
1986; Isler and Isler 1987); tanagers often
reach-down alternately on opposite sides
of a branch as they move along thebranch, as does the wren Odontorchilus
brunt&ii (Parker et al. 1980). A bird-ofparadise (Purotiucarolue)apparently uses
a similar maneuver when searching

BIOLOGY

NO.

13

branches (Forshaw and Cooper 1979). At
least one hummingbird (Metalluru tyrianthina) uses reach-down maneuvers
to reach more than a third of its flowers(Remsen 1985).
3. Hang: to use legs and toes to suspend the
body below the feet to reach food that cannot be reached from any other perched position. “Hang-glean” of Recher et al. (1985)
and Robinson (1986) is a synonym. Differences in frequency of use of “hang” among
similar species may have subtle consequences for morphology (Partridge 1976a,
Leisler and Thaler 1982). Parrots use “hana”
frequently (Forshaw 1973 and references
therein). Chickadees and titmice (Paridae),bushtits (Aegithalidae), and some thornbills(Acanthizu) frequently “hang” to reach undersides of branches and leaf tips (e.g., Gibb
1954: Root 1964. 1967: Grant 1966: Sturman 1968; Partridge 1976b; Rabenold 1978;
Moreno 1981; Alatalo 1982; Bell 1985b;
Recher et al. 1985, 1987; Laurent 1986).
The Palm Tanager (Thraupispalmarum) in
Trinidad “hangs” almost exclusively whensearching for insects in foliage (Snow andSnow 1971). The Blue-backed Conebill(Conirostrum sitticolor; Thraupinae) alsouses this maneuver as its primary means ofattack (Remsen 1985). Other insectivores
that use “hang” regularly include: Rufousbrowed Wren (Troglodytes rufociliatus;
Skutch 1960), some wood-warblers (Root
1967, Fickenand Ficken 1968, Elliott 1969,
Andrle and Andrle 1976, Rabenold 1980),
Speckled Tanager (Tanguru guttata; Snow
and Snow 197 1); some white-eyes (Zosterops;Gill 197 1, Earl& 1983); Ruby-crowned
Kinglet (Regulussatrupa; Rabenold 1978);the fumariid Siptornis striuticollis(Eley etal. 1979); and Sharpbill (Oxyruncuscristatus; De L. Brooke et al. 1983, Stiles andWhitney 1983). Some vireos “hang” whengrasping the margins of leaves to reach foodthat cannot be reached from branches (Vireo
griseus,Nolan and Wooldridge 1962; V.
huttoni and V. gilvus, Root 1967); several
tropical vireos (Hylophilus)use this maneuver frequently if not predominately (Greenberg 1984a; T. A. Parker and JVR, unpubl.
data). Many species that extract prey fromhanging dead leaves “hang” (and “reach”)
to investigate isolated dead leaves (Skutch
1969 for Automolus ochrolaemus;Greenberg 1987b; K. V. Rosenberg, unpubl. data;
JVR, unpubl. data). Among frugivores that“hang” to reach fruit are Euphonia violucea(Snow and Snow 197 1) and two species ofwoodpeckers (Moermondand Denslow
1985). Several hummingbirds “hang” toreach flowers (Parker and O’Neilll980,
Parker and Parker 1982, Parker et al. 1985,
Remsen 1985). Four types of “hang” maneuvers (Fig. 1) should probably be distinguished (modified after Partridge 1976b,

CLASSIFICATION

OF BEHAVIOR--Remsen

and Robinson

Rabenold 1980, Alatalo 1982, Earl& 1983,
and Greenberg 1987b):a. Hang-up: to hang, head-up.
b. Hang-down: to hang, head-down. Thisdiffers from reach-down only in that thebird is clinging to a vertical surface orside of a horizontal surface, rather thanperching on the upperside of a surface inreach-down. There is probably a continuum between the two maneuvers, and infact, Moermond and Denslow’s (1985)“reach” would include maneuvers here
considered to be “hang-down.”c. Hang-sideways:to hang on the side of a
substrate with body axis parallel to theground and with the bird’s side oriented
upwards.
d. Hang-upsidedown:to hang, belly-up, on
underside of horizontal or diagonal surface.
These same four categories may also be applied to
the foraging behavior of all specialized bark-foraging
birds (e.g., woodpeckers, dendrocolaptids, certhiids) thatcharacteristically hang while searching and attacking;in bark-foraging birds, these maneuvers are probably
best considered postures rather than maneuvers.
4. Lunge: those maneuvers in which the food
item is beyond the range of “reach,” butrapid leg movements rather than flight areused to approach and capture the prey. Thisis synonymous with the “lunge” of Greenberg (1984a), except that Greenberg’s lunge
would include movements that we call“reach-out.” Root’s (1967) “rush” is a combination of our “sally-pounce” (see below)
followed by our “lunge.” Some studies haveused “dart” for foliage-gleaning birds and“rush” for ground-foraging birds as presumed equivalents. Several ground-foraging
birds, particularly thrushes (Heppner 1965;
Smith 1973; Tye 1981; Willis 1985a, 1986)
and ground-cuckoos (Neomorphus:Willis
1982a), and also some bulbuls (Bleda;Willis
1983a), tyrannids (Muscisaxicola,Smith andVuilleumier
197 1; Corythopis torquata,
Willis 1983b), and antbirds (Gymnopithys,
Willis 1968; Grallaricula nana, Parker et al.
1985) use the lunge maneuver regularly. Arboreal birds that also regularly lunge include: Red-crowned Ant-Tanager (Habia
rubica; Willis 1960), Plain-brown Woodcreeper (Dendrocincla fuliginosa; Willis
1972), Chestnut-crowned Gnateater (Conopophaga castaneiceps;Hilty 1975); Blackheaded Grosbeak (Pheucticusmelanocephalus;Airola and Barrett 1985), the tiny, canopy antwrens of the Terenura callinota superspecies (Remsen et al. 1982; Stiles 1983;
T. A. Parker, unpubl. data), White-shouldered Tanager (Tachyphonus luctuosus;
Greenberg 1984a; JVR, unpubl. data), andan undescribed species of Cercomacra(Formicariidae; Parker and Remsen 1987).

FIGURE 1. “Hang” maneuvers: (a. 1) = “hang-up”
on vertical perch, (a.2) = “hang-up” on horizontal perch,(b. 1) = “hang-down” on vertical perch; (b.2) = “hangdown” on horizontal perch; (c) = “hang-sideways”; (d)= “hang-upsidedown.” Drawing by Donna L. Dittmann.
B. Subsurface maneuvers (bird penetrates or manipulates the substrate rather than removing
food from its surface; the attack is directed atfood that cannot be seen from the surface without substrate manipulation).
1. Probe:to insert the bill into cracks or holes
in firm substrate or directly into softer substrates such as moss or mud to capture hidden food. This tactic is often associated withspecialized morphologies adapted for specific substrates. Most probers have long,
slender, decurved bills for reaching deep into
crevices, tubes, holes, and soft substrates
such as mud or moss. Those that probe barkoften have specialized hindlimb morphology and tail structure for climbing on andbracing against branches (Richardson 1942,
Bock and Miller 1959, Feduccia 1973, Norberg 1979). Several unrelated groups have
converged on similar morphology associated with bark probing: the creepers (Certhiidae), some woodcreepers (Dendrocolaptidae), and the Australian
treecreepers(Climacteris spp.). The scythebills (Campylorhamphus spp.) and the Long-billed
Woodcreeper (Nasica longirostris), withsome of the longest bills relative to bodysize of any passerines, use their bills forprobing deep into holes in tree trunks and150

STUDIESIN AVIAN

bamboo stems and into large bromeliad
clusters (Pierpont 1986; T. A. Parker, unpubl. data; JVR, unpubl. data). Some woodpeckers do more probing (and gleaning) thanthe more “typical” woodpecker maneuvers,
such as “peck” and “hammer” (e.g., Bock
1970; Short 1973, 1978; Cruz 1977; Alatalo
1978; Cruz and Johnston 1979, 1984; Stacey 1981; Askins 1983; Pettersson 1983;.Kattan 1988). Bark-foraging birds that also
probe epiphytic vegetation include theBrown Creeper (Certhia familiaris; Stiles
1978), many woodcreepers (Willis 1983c,d), and some woodpeckers (Kilham 1972,
Short 1973, Cruz 1977, Askins 1983) andcertain fumariids (Skutch 1969, Eley et al.
1979, Parker et al. 1985, Remsen 1985).
Some species without obvious morphological adaptations for climbing also frequently
probe bark or epiphytes on branches. Although examples include continental birds,
such as the Sharpbill (Stiles and Whitney
1983), some wrens (Root 1964, Parker
1986a), and the Red Warbler (Ergaticus
tuber;Elliott 1969) they are particularly frequent on islands or in regions such as New
Guinea and Australia where specializedbark-searching taxa are rare or absent (Keast
1968, Zusi 1969, Cruz 1978). Examples include: a pachycephalid (Colluricincla harmonica),a scrub-wren (Sericornismagnus),
and some meliphagid honeyeaters (Keast
1968, Recher et al. 1985); a mimid (Cinclocerthia rufcauda; Zusi 1969); some Hawaiian honeycreepers (Richards and Bock 1973);
some ictetids (Nesopsarnigerrimusand Icterus leucopteryx;Cruz 1978); and several
birds-of-paradise(Ptiloris spp., Astrapia

mayeri, Pteridophora alberti, Diphyllodes
magnijicus; Forshaw and Cooper 1979).
Many speciesthat search hanging dead leaves
for hidden arthropods probe into these curled
leaves (Remsen and Parker 1984 and references therein; K. V. Rosenberg, unpubl.
data; T. A. Parker, unpubl. data). Similarly,
some species of small tanagers (Dacnis spp.
and Cyanerpesspp.; Snow and Snow 197 1,
Isler and Isler 1987) use their slender bills
to probe inside curled living leaves. Some
populations of Yellow-throatedWarbler(Dendroica dominica) probe pine cones(Ficken et al. 1968, Emlen 1977) or denseclusters of pine needles or small leaves (Lackand Lack 1972). Some ground-foraging birds
probe in soil, mud, or deep leaf-litter; examples include thrashers (Toxostoma,
Mimidae; Fischer 1981), White’s Thrush(Zoothera dauma; Edington 1983), Rook
(Corvusfrugilegus; Waite 1984b), Whitewinged Chough (Corcorax melanorhamphos;Ford et al. 1986), and the woodcocks(Scolopaxspp.; Sheldon 197 1). The furnariid Cinclodesexcelsiorprobes moss and lichens on rocks and the ground (Fjeldsa etal. 1987). Hundreds of species of nectar-

BIOLOGY

NO.

13

feeding birds around the world probe flowers, especially in the Trochilidae, Nectarinidae, and Meliphagidae. Woodpeckers andhummingbirds also extend their tongues toprobe crevices, holes, and flowers; suchprobing could be labelled “tongue-probing.”
C. Subsurface maneuvers with SubstrateManipulation (maneuvers in which the substrate is
manipulated beyond insertion of a probe).
1. Gape:to insert the bill into the substrate as
in a probe, but the bill is opened to widen
the opening. This maneuver is characteristicof many starlings and American blackbirds(Icteridae), which have bills and jaw musculature adapted for gaping (Beecher 195 1,
1978; Orians 1985b). Various icterids use
their bills to open holes in curled living anddead leaves (e.g., orioles [Icterusspp.]), deadbranches and stems, moss, bromeliad clusters, seed clusters, leaf-litter, soil (Sturnellaspp.), clumps of grass, flowers, and large
fruits (Cruz 1978; Orians 1985b; Robinson
1985, 1986, 1988); they also use “gape” toturn over stones, twigs, dung, and other objects that might conceal prey on the ground(Orians 1985b). Several species of woodwarblers, including several Vermivora spp.
(Ficken and Ficken 1968), the Swainson’s
Warbler (Limnothlypisswainsonii;Meanley1970), and the Worm-eating Warbler (Helmitherosvermivorus;Greenberg 1987b), use
the gape maneuver for probing buds, deadleaves, and flowers. The Sharpbill “gapes”
to open tightly rolled young leaves and deadleaves (Stiles and Whitney 1983), as does
the woodhoopoe Phoeniculusbolleito open
crevices in loose bark (Liihrl 1972). Instances of gaping are occasionally reported
in other taxa, such as Meliphagidae (Keast
1968) and Dendrocolaptidae (Willis 1983~).
2. Peck: to drive the bill against the substrate
to remove some of the exterior of the substrate. This maneuver is characteristic ofmany woodpeckers (Picidae) that excavateholes in bark or wood to expose prey. “Peck”
is synonymous with the “tap” maneuver ofsome studies of woodpeckers; we recommend restricting “tap” to those motions thatare probably exploratory pecks for detecting
wood-borer tunnels or movements, as described by Davis (1965) and Kilham (1972).
Many parids and at least one icterid (Nesopsarnigerrimus;Cruz 1978) also peck to
excavate holes in rotted wood. Ground-foraging birds use this maneuver in combination with “flake” (see below) to dig small
holes to reach food in the ground (e.g.,thrashers [Toxostoma], Engels 1940, Fischer 198 1; and some thrushes, Tye 198 1).
Some frugivorous birds use “peck” to breakthe outer skin of large fruit (Snow and Snow
197 1). The Bananaquit (Coerebaflaveola;
Gross 1958), some hummingbirds (Colwell
1973, Stiles 1985c), some white-eyes (Zos-CLASSIFICATION

OF BEHAVIOR--Remsen

terops; e.g., Gill 1971) and icterids (Robinson, unpubl. data) may use this maneuver,usually described as “piercing,” to make ahole in the base of flower corollas for “stealing” nectar, but the actual maneuver used
to make the hole is uncertain. The flowerpiercers (Diglossa) hold the flower with theirhooked upper mandible and pierce with their
sharp, upturned lower mandible (Skutch1954).
3. Hammer: to deliver a series of pecks without pausing between pecks. This maneuveris mainly restricted to certain woodpeckers
that use it for excavation of deep holes toreach bark- or wood-dwelling insects or sap.
The twig-foraging furnariid Xenopsminutus
also uses this maneuver frequently (Skutch1969). Some chickadees and titmice (Paridae) may use this maneuver occasionally toopen acorns, galls, seeds, and fruits (e.g.,
Parusinornatusand P. rufescens;
Root 1964,1967), but the pecks are not delivered as
rapidly as in woodpeckers. The distinction
between hammer and peck, which rests onwhether there is a pause between pecks, may
be vague. Counting the number of pecks perunit time, and thereby eliminating the“hammer” category, is an alternative treatment.
4. Chisel:like “peck,” but rather than the bill
being pounded almost perpendicularly into
the substrate, it is aimed more obliquely at
the substrate-usually bark or dead stemsand the bill is used as a chisel or lever todislodge portions of the substrate. The direction of head movements is forward andupwards. Slightly to strongly upturned lower mandibles that give the bill a somewhat
chisel shape are often associated with species
specialized on chiseling. Species that seemto have converged on this foraging behavior
and morphology are some Xenops spp. (Furnariidae: Skutch 1969). the dendrocolautid
Glyphor$nchusspirur& (Skutch 1969),-thefumariid Simoxenopsucayali (JVR and T.
A. Parker, unpubl. data), and the antbird
Neoctantesniger (Hilty and Brown 1986);
and to a lesser degree, nuthatches (Sit@ spp.)
and sitellas (Sitellu spp.; Holmes and Recher 1986a, b). We invented this category tomatch our expectations of how chisel-shaped
bills are used rather than on any data on
movements used by these species. Althoughsome brief descriptions (e.g., Glyphorynthus; Skutch 1969) fulfill our expectations,the reality of our “chisel” maneuver remains unclear.
5. Flake: to brush aside loose substrate withsideways, sweeping motions of the bill. Not
as much force is required as in chisel or pry
because the substrate dislodged is alreadyloose or unattached. This category combines two types of motions that are often
difficult to distinguish in the field: the closed
bill tip is used to brush aside the substrate,and Robinson

151

and the substrate is grasped briefly between
the mandibles (which can be called “toss”
when the distinction can be made). “Flake”
is synonymous with “bill-sweeping” (Clark
1971) except that it applies to substrates
other than leaf-litter. “Flake” is also auuarently synonymous with R. J. Craig’s (i 984)
“leaf-pull.” Many bark-foraging woodpeckers “flake” to dislodge loose sections of bark(Tanner 1942; Kilham 1965, 1983; Conner1981). The term “scaling” used in manystudies of woodpeckers to describe removalof loose bark presumably refers to a combination of our “pecking,” “flaking,” and“prying.”
Some dendrocolaptids(Willis1983c, Pierpont 1986) fumariids (JVR, unpubl. data), and a meliphagid (Melithreptus
brevirostris;Keast 1968) use this maneuver
to search through debris clusters and loose
bark. Ground-foraging
birds that “flake”
leaf-litter include some thrushes (Turdus[Skutch 1960, 1981; Clark 1971; Tye 19811;
kylocichla [Clark 197 1; Holmes and Robinson 19881: Alethe [Willis 19861). antbirds(Formica&, Skutch 1969, Wiihs 1985b,
Rhopornis,Willis 198 la), leaftossers (Sclerurus, Furnariidae; Skutch 1969, Hilty and
Brown 1986) thrashers (Toxostoma;Clark
197 1, Fischer 198 l), bulbuls (Bleda; Willis
1983a), the waterthrushes (Seiurus; R. J.
Craig 1984) and homeros (Furnarius;Robinson, unpubl. data). The Dune Lark (Mirafra erythrochlamys)uses “flake” to dislodge sand to excavate small craters to expose
hidden seeds(Cox 1983). The fumariid Cinclodesexcelsior“flakes” moss and lichensfrom rocks (Fjeldsa et al. 1987).
6. Pry: to insert the bill into a substrate anduse it as a lever to lift up portions of thesubstrate. This differs from “flake” in thatthe sides of the bill, rather than the tip, accomplish the movement of the substrate
while the tip remains relatively stationary.
Substrates for which “pry” is needed are
generally more firmly attached than thosedislodged when a bird “flakes.” “Pry” differs from “chisel” in that the tip of the billis stationary, instead of moved forward andupward as in chisel. Examples of species
that use “pry” are: Band-backed Wren
(Camuvlorhvnchuszonatus: Skutch 1960).
some- species of dendrocolaptids (Skutch
1945; Willis 1983c, d), a meliphagid (Melithreptus validirostris;Keast 1968) many
woodpeckers (e.g., Short 1973) and a birdof-paradise (Astrupia mayeri; Forshaw andCoouer 1979).,_all of which urv-_ UD_ sectionsof loose bark, and Sharpbill, which pries
moss from branches (Stiles and Whitney
1983).
7. Pull: to grasp, pull, or tear, and thereby remove or dislodge sections of the substratewith the bill. Pullina differs from “flakina”
in that the target substrate is grasped in thebill because extra force is needed to dislodge

152

STUDIESIN AVIAN

more firmly attached potions of substrate.
Birds that pull off loose bark or lichens to
attack hidden insectsinclude Band-backed
Wren (Skutch 1960) Plain Titmouse (Purusinornatus; Root 1967), Crested Shrike-Tit(Falcunculus fiontatus: Recher et al. 1985.
Ford et al. 1986), a bird-of-paradise (Mac:gregoria pulchra ; Forshaw and Cooper1979), some orthonychids (Holmes andRecher 1986a), some dendrocolaptids(Willis 1983c, d) and Giant Cowbird (Scuphiduru orvzivoru: Robinson 1988). The Plain
Titmouse also pulls apart leaf galls, flowers,
lichens,and curled dead leaves(Root 1967).
Thrioadectes rufobrunneus (Skutch 1969)and several other fumariids (T. A. Parker;
unpubl. data) pull leaves from bromeliads
to expose prey. Most New World barbets(Cupito, Eubucco) also pull open large deadleaves, twig galls, and sections of rotting
wood to searchfor prey (Remsen and Parker
1984;T. A. Parker, unpubl. data; SKR, pers.
obs.). The Plush-cappedFinch (Catamblyrhynchus) pulls the leaf whorls at the nodes
on bamboo stems, presumablyto reveal insects(Hilty et al. 1979, Remsen 1985). The
ground-foragingSong Thrush (Turdus philomelos) uses “pull” in its foraging repertoire (Henty 1976). Many parrotsuse“pull”
for openingfruits, seeds,flowers,and rotting
wood (Forshaw 1973 and referencestherein).
8. Scratch: to dislodgesectionof substratewithfoot movements. This maneuver is usedby
many ground-foraging birds around theworld; examples include: some orthonychids (Zusi 1978, Frith 1984), Australianlyrebird (Menuridae; Recher et al. 1985,
Holmes and Recher 1986b), and some
megapodes (e.g., Alectura lathami; Frith
1984). Although most speciesscratchusing
one foot at a time, many emberizid sparrows(Davis 1957, C. J. 0. Harrison 1967, Hailman 1973, Greenlaw 1976 and references
therein) and occasionally some thrushes(Turdus; Clark 1983) and icterids (Greenlaw1976) move both feet simultaneouslyto expose food under leaf-litter or snow.
II. Aerial maneuvers (bird must leave substrate toreach food)
A. Leg-powered maneuvers
1. Leap: to launch into the air to reach a food
item too far for a “reach” but too close fora “sallv.” This differs from “sally” in thatthe upward thrust seems to come mostly
from leg movements rather than wing
movements (Davies and Green 1976); it isequivalent to the “jump-glean” of Holmes
and Robinson (1988) and presumably the“jump” of Hutto (198 1b). Distinguishing“leap” from short sallies is often difficult.
Davies and Green (1976) found that “leap”
was the most frequent maneuver used byReed Warblers (Acrocephalus scirpaceus),and Greenberg (1984a) found that it com-

BIOLOGY

NO. 13prised 25% of the maneuvers of Chestnutsided Warblers (Dendroica pensylvanica) inwinter. Holmes and Robinson (1988) foundthat about one-fifth of all maneuvers usedby Ovenbirds (Seiurus aurocapillus) andDark-eyed Juncos (Junco hyemalis) wereleaps.Greenbergand Gradwohl(l980) considered leaping (from ground to foliage) tobe the primary foraging maneuver of Kentucky Warblers (Oporornis formosus) and
Chestnut-backed Antbirds (Myrmeciza
exsul). The Chestnut-crowned Gnateater(Conopophaga castaneiceps) leapsto nearby
perches to attack prey (Hilty 1975). Many
speciesthat follow army-ant swarms probably “leap-down” from low perchesabove
the ants to capture flushed insects (e.g.,
Gymnopithys, Willis 1968;Rhegmatorhina,
Willis 1969; Phfegopsis, Willis 198 1b; Dendrocincla. Willis 1972. 1979).
, Some seedeating speciesapparently leap onto stemsto
pull seedheadsto the ground (Emlen 1977).
The directionand distanceof the leap should
be recorded,just as it is for “sally” (seenext
account), particularly because a “leap”
downward (i.e., dropping)probably requires
only a fraction of the energy than does anupward or outward leap againstgravity.
B. Wing-powered maneuvers
1. Sally: to fly from a perch to attack a food
item (and then return to a perch). Most authors have used separate terms to distinguishsalliesdirectedat aerialprey from those
aimed at nonflyingprey. We do not, because
the foraging site (i.e., air vs. anything else)
will automatically be recorded more appropriately in our schemeunder the “substrate”
category(see below); and the maneuver itself appearsto us to be very similar whether
directed at air or hard substrate.Although
we acknowledge that the movements directed at flying vs. nonflying food may bedifferent, we prefer to remove the substratebias from terminology as much as possible.
Another difference between our systemand
othersis that the term “hawk” hasbeen usedfrequently to describe what we here call“sally” (e.g., Holmes et al. 1979b). We use“sally” rather than “hawk” because:the dictionary definition of “sally” is closer to thisbehavior than is “hawk,” and hawks rarely
if ever fly from a lookout perch to attack
flying prey. Similarly, the term “flycatch”
has been used frequently for sallies after
flying prey, but most “flycatchers,” whether
tyrannids or muscicapids,do not “flycatch”
perse, but insteadgleanor sallyto substrates(e.g., Fitzpatrick 1980). Greenberg (1984a)
distinguished sallies in which a bird returned to the perch from those in which thebird continuesin the samedirection by calling the latter “darts.” There is probablymore
among-author variability in terms used todescribeaerial maneuvers (e.g., hawk, hover, hover-glean, snatch, sally, flycatch) than

CLASSIFICATION

OF BEHAVIOR--Remsea

in any other broad category of foraging behavior.
Many species have characteristic directions or distances associated with their sallies that provide an index of the average search radius (Fitzpatrick 1981,
Robinson and Holmes 1982) and these arc importantto record (after Fitzpatrick 1980):
a. sally-distance (distance of the sally fromperch to food item).
divisionsb. sally-angle (the qualitative“UP, ” “down, ” “horizontal,” “diagonalup,” and “diagonal-down” probably represent maximum possible resolution under most field conditions). Certain species
or species groups may have characteristic
sally angles. Willis (1984), for example,
noted that most manakins (Pipridae)
typically sally only at a horizontal angle,
and Holmes and Recher (1986a) foundthat two species of thornbills differed in
the angles of their sallies.
Sally-distance and sally-angle should refer to the initial attack attempt only; subsequent pursuit of a missed
target should be recorded separately. We distinguishfive types of sallies based on the bird’s foraging motion
at the end of the sally:a. Sally-strike: to attack in a fluid movement without gliding, hovering, or landing (after the “outward striking” and“upward striking” of Fitzpatrick [ 19801
and the “snatch” of Moermond andDenslow [1985]). The “sally-strike,”
whether aimed at flying prey or stationary substrates, is the characteristic attack
behavior of many Tyrannidae (Hespenheide 1971; Fitzpatrick
1980, 1985;
Sherry 1984), Muscicapinae and other
Old World “flycatchers” (e.g., Croxall
1977, Davies 1977b, Fraser 1983, Moreno 1984), Pipridae (Skutch 1969), Bucconidae (e.g., Skutch 1948; Willis 1982b,c), Galbulidae (Hilty and Brown 1986)
Meropidae (Fry 1984) Momotidae (e.g.,
Skutch 1947; Willis 198 lc), Alcedinidae(Fry 1980), and Conopophagidae (Willis
1985b). Numerous species in other families use the sally-strike maneuver tovarying degrees, accompanied by morphological adaptations that parallel thoseseen in more typically sally-striking
groups (Partridge 1976b, Norberg 1979,
Schulenberg 1983). Most species that use
this maneuver are sit-and-wait predatorsthat watch for prey while sitting motionless on an elevated perch, although others search more actively (e.g., tree-climbingdendrocolaptids [Willis 1972, 1982d,
Pierpont 19861 and some vireos [Robinson and Holmes 19821). Ground-foraging birds that “sally-strike” to capture
insects on foliage above them include thetyrannid Corythopis torquata (Fitzpat-

and Robinson

153

rick 1980, Willis 1983b) and Catharus
thrushes (Paszkowski 1984, Holmes andRobinson 1988). Other ground-foraging
birds “sally-strike” to catch flying insects. Examples include ground-tyrants(Muscisaxicola spp. [Smith and Vuilleumier 1971; Fitzpatrick
1980, 1985]),
Rhipidura leucophrys (Ford et al. 1986),
and wheatears (Oenanthe spp.; Leisler andSeinbenrock 1983). Some species also use
this maneuver to obtain fruit (Skutch
1969; Fitzpatrick
1980, 1985). Sallystriking species often have wide, scooplike bills and wide gapes that presumably
facilitate prey capture in flight (Fitzpatrick 1985).
b. Sally-glide: like sally-strike except the final approach at the target is a glide (vs.
continuous flapping in sally-strike).
Moermond and Denslow (1985) pointed
out that many sally-strikers do not use
continuous, flapping flight in their approach, and they made a convincing casefor distinguishing those species that useda brief glide from those that did not. It
is likely that some or many of the examples of sally-strikers above are actually sally-gliders. Other than Moermond and Denslow’s (1985) data on
frugivores, the prevalence of sally-gliding(which they called “sally-scooping”) vs.
sally-striking will be revealed only by
careful observations.
Sally-stall: to stall in front of the target
briefly with fluttering motions at the endof the sally. Moermond and Denslow(1985) noted that many species usuallyconsidered to sally-hover (see below) do
not engage in true hovering (flying inplace), but rather flutter awkwardly in astalling motion after a steep attack angle
at the final approach of the sally. Suchspecies, mainly trogons and some cotingas, use different flight motions and havedifferent morphological adaptations fromthose that hover. We suspect that manyof the examples of “sally-hover” noted
below may actually be “sally-stalling.”
As with sally-gliding, only careful observations (or high-speed photography?) will
reveal its true prevalence among sallying
birds.
Sally-hover: like other sallies except thatthe bird hovers at the target substrate at
the end of the sally. This is synonymouswith Fitzpatrick’s (1980) “hover-glean.”
Most studies do not distinguish between
sally-strike and sally-hover (much lesssally-glide and sally-stall), and many other studies appear to label all sallies tofoliage as “hovering” (e.g., Holmes et al.
1979b), even though few of these maneuvers actually involve hovering flight.
Unless these maneuvers are distinguished, the possibility that they require

154

STUDIESIN AVIAN

different morphological adaptations, as
found for frugivores by Moermond andDenslow (1985), cannot be addressed.
Some tyrannids use the sally-hover maneuver regularly (Fitzpatrick 1980, 1985),
as do kinglets (Regulus;Rabenold 1978,
Moreno 198 1, Franzreb 1984) the Bluegray Gnatcatcher (Polioptila caerulea;
Root 1967) some sylviid warblers (Phylloscopus;Gaston 1974) some woodwarblers (Ergaticus ruber, Elliott 1969;
Dendroica. Rabenold
1978.
1980:
Greenberg 1984a); an acanthizid (Sericornis magnirostris; Frith 1984), theRestless Flycatcher (Myiagra inquieta;
Ford et al. 1986), and some putlbirds(Sherry and McDade 1982; Willis 1982c,e). Bell (1984) found that at a forest sitein New Guinea, 5 of 83 bird species studied in detail used this maneuver in 1824% of his foraging observations: two(Monarcha andmonarch-flycatchers
Arses),a cracticid (Peltops),a meliphagid(Melilestes), and a drongo. Similarly,
Remsen (1985) found that at a forest site
in the Andes, 4 (all tyrannids) of 33
species studied in detail used this maneuver in 16-33% of their foraging observations. In contrast, hovering accounted for only 1% of all prey attacks
observed in an Australian eucalypt forest
where 41 species were studied in detail(Recher et al. 1985). Many species use
this maneuver when taking fruit. Examples include many tyrannid flycatchers, manakins, and some tanagers (Fitzpatrick 1980, Willis 1984, Moermondand Denslow 1985). Some species, including kinglets (Leisler and Thaler 1982,
Franzreb 1984) some wood-warblers(Morton 1980a), and the Yellow-rumped
Cacique (Robinson 1986), occasionallyhover under surfaces to search for foodthat cannot be seen from a perch. Hummingbirds, of course, use this maneuver
extensively when feeding at flowers or
searching foliage and branches; for nectar-feeding,however, the parameters“sally-distance”
and “sally-angle”
areusually irrelevant.
e. Sally-pounce:to land briefly at the endof the sally to take food from substrate.
Although the bird is perched when it takes
the food item, we classify this maneuver
as a “sally” because it involves a flightafter food is spotted at a distance fromthe lookout perch. It is probably synonymous with Fitzpatrick’s(1980)“landing-and-gleaning,”
Recher et al.‘s(1985) “pounce,” and Holmes and Robinson’s (1988) “dive-glean.”
Examplesofbirds that use this maneuver are: many
open-country tyrannids and muscicapids(Fitzpatrick 1980, 1985; Fraser 1983),
bluebirds (Power 1980) Australian robins (Petroica, Eopsaltria; Recher et al.

BIOLOGY

NO.

13

1985, Ford et al. 1986, Holmes and Recher 1986b), and Fan-tailed Cuckoo (Cuculuspyrrhophanus,Recher et al. 1985),
some Catharus thrushes (Dilger 1956,
Paszkowski 1984), some pullbirds (Willis 1982b, c), and the Field (Spizella pusilla) and Chipping (S. passerina)sparrows when foraging for insects (Allaire
and Fisher 1975). Some vireos (Vireonidae) use this maneuver when attacking
prey on branches (James 1976, Robinson
and Holmes 1982). Some tropical vireos(Hylophilus) characteristically use thismaneuverfollowed immediatelybyhanging on leaf margins when attacking
undersides of leaves (T. A. Parker and
JVR. unwbl. data). A soecial kind of
sally:pounce is used by some seed-eating
birds that sally to a grass stem, grasp thestem in their feet, and then allow theirweight to pull the stem to the ground,
where seeds can be removed more effectivelv (Allaire and Fisher 1975).
Flutter-ktase: to flush or dislodge prey froma substrate and to then chase the prey. Thismaneuver is used regularly by foliage-gleaning birds that flutter after a falling or flying
prey item that has escaped their normal attack behavior and is often preceded by alunge. Root’s (1967) “tumble” is synonymous (because “tumble” refers to out-ofcontrol, sommersaulting movements, wehave chosen a new term). Root (1967) foundthat Blue-gray Gnatcatchers (Polioptila caerulea) used this maneuver in 23% of all sallies directed at insects in the air; however,Root suspected that the frequent tail-flashing of this species may function to startle
insects, therefore making these “flutterchases” into “flush-pursuits” (see below) in
our scheme. Morse (1968) found that fourwood-warblers (Dendroica) used this maneuver in about 5% of their foraging motions. We see this maneuver most frequently
in foliage-gleaning birds in mixed-species
flocks in the canopy of tropical forests; apparently, the escape behavior of many of
their arthropod prey involves falling fromthe substrate at the approach of a bird predator. In particular, the White-shouldered
Tanager (Tachyphonusluctuosus)uses theflutter-chase maneuver frequently (Snow andSnow 1971; JVR, unpubl. data). We use thisterm mainly for species that are not typicallysalliers. We recomend recording the distance and angle of the chase, just as in thesally maneuvers.
Flush-pursue:similar to “flutter-chase” except that species that use this maneuver deliberately (vs. accidentally) flush prey fromhiding places and then pursue the flying or
falling prey. This maneuver tends to beprominent in the foraging repertoire of
species that use it, most of which have conspicuous wing or tail spots or stripes thatare flashed to startle hidden prey. Distin-CLASSIFICATION

OF BEHAVIOR--Remenguishing this maneuver from “flutter-pursuit” may be difficult, but because each involves fundamentally different tactics, we
believe that to do so where possible is valuable. Among North American species, theAmerican Redstart (Setophaga ruticilla;
Robinson and Holmes 1982) and, on the
ground, the Northern Mockingbird (Mimus
polyglottos;Hailman 1960) most frequently
use this maneuver. Other examples include:
Dendrocincla woodcreepers (Willis 1972,1979) fantails (Rhipidura; Recher et al.
1985, C. J. 0. Harrison 1976, Holmes andRecher 1986a), Monarcha flycatchers (Pearson 1977b), Myiobiustyrannids (Fitzpatrick1980) Ruddy-tailed Flycatcher (Terenotriccuserythrurus,Sherry 1984), and the Myioborusredstarts (Parulinae; Remsen 1985).
4. Screen:to attack in continous flight (afterEmlen 1977, Fitzpatrick 1980). (Note that
this is a searching behavior as well as an
attack maneuver.) This is synonymous with“hawk” as used by Remsen (1985) and others for birds that feed in flight. Swallows,
swifts, and nighthawks (Chordeiles,Caprimulgidae) use this maneuver almost exclusively. Other birds that may use this maneuver occasionally
include European
Starling (Sturnusneglectus;
Cayonette 1947)
Golden-naped Woodpecker (Melanerpes
chrysauchen;Skutch 1969) Lewis’ Woodpecker (M. lewis; Bock 1970), some tyrannids (Fitzpatrick 1980) and probably the
pullbird Chelidoptera tenebrosa (Burton1976).
FORAGING

SITE

We suggest recording the following parameters withrespect to the foraging site used by a foraging bird: (1)general habitat, (2) vertical position, (3) horizontal position, (4) foliage density, and (5) the precise substratefrom which the food was taken. We discuss each catgory briefly.
I. Habitat: Many study areas contain more than one
habitat or microhabitat. Each foraging record
should be assigned to one of the investigator’s
general habitat or microhabitat categories to permit examination of the influence of habitat onforaging behavior (e.g., Bilcke et al. 1986). Classification of habitats, a complex and critical topic,
is beyond the scope of this paper.
II. Vertical position: It has been recognized for decades that important differences in vertical position separate the foraging activities of many closely
related birds. Furthermore, foraging behavior may
change with changes in height above ground.
Therefore, every foraging record should be assigned two values to allow its position to be plotted: (1) height-above-ground and (2) distance-tocanopy (above bird). We have also found a thirdparameter to be of interest: (3) height of the individual plant in which the bird was foraging. This
allows us to distinguish species that frequently use
small trees or saplings within the foliage column
from those that use the lower foliage of canopy

and Robinson

155

trees at the same height as the small trees. Provided that only one observer records the data, avisual estimate of height (vs. precise measurements) may be the only practical way to obtainsuch data. Not only does the time required tomake precise measurements reduce the volumeof data that can be collected, but it seems unlikelythat the birds recognize vertical subdivisions sufficiently precisely to warrant such a time investment. Heterogeneity in canopy height, light penetration, and foliage distribution obliterate such
precise boundaries. However, differences amongobservers in the accuracy of such visual estimates(Block et al. 1987) reveal the unreliability of suchvisual estimates and provide support for use ofobjective measures of height.
III Horizontal position: Many researchers have recorded the “horizontal” position (e.g., “inner,”“middle,” “ outer”) of the bird in the tree or bush.
Many species of foliage- and branch-gleaning birds
characteristically favor one ofthese foraging zones(e.g., MacArthur 1958 and numerous other studies). Whether birds select such zones per se,or are
keying on differences in foliage density (next category) is unknown. It is possible that “horizontal
position” and “foliage density” measures arelargely redundant. However, Greenberg and
Gradwohl (1980) and Holmes and Robinson(198 1) showed the importance of branch and leaf
arrangement around the bird in determining whichsurfaces can be attacked effectively. Greenberg(1984a) used a system for “horizontal” position
designed specifically to place the foraging bird in
categories with respect to foliage and branch geometry.
IV Foliage density:Foliage density at the point offoraging- - observation can be recorded using a qualitative scale. For example, the system that-we havefound to be useful (ea..
. __ Remsen 1985: modified
from Wiley 197 1) is a scale from “0” to “5” ofincreasing foliage density within a one-meter radius around the bird: “0” = no vegetation within
the imaginary l-m sphere; “1” = very low vegetation density within the sphere (e.g., 95-99% of
all light passes through sphere); “2” = low density,
75-95% of light passes; “3” = moderate density,
25-75% of all light passes; “4” = high density,
only 5-25% of light passes; and “5” = extremely
dense, O-5% of light passes.
V. Substrate. We have found the following substratecategories to be useful:
A. Living Foliage
1. Plant speciesor “type” (species, genus, orfamily when possible; otherwise “broadleaf tree,” “vine,” “palm,” “grass,” “bamboo,” “fern,” “ cactus,” and the like; note
if epiphytic). Many studies (e.g., Hartley
1953; Gibb 1954; Willson 1970; Reller
1972; Holmes and Robinson 198 1; Woinarski and Rounsevelll983; Robinson andHolmes 1984; Franzreb 1984; Bell 1985b;
Morrison et al. 1985, 1987b) have emphasized the importance of distinguishing plant
species. In the tropics, many bird species
specialize on distinctive plant types such

156

STUDIESIN AVIAN

as bromeliads,
bamboo (Parker 1982,
Remsen 1985) and palms.
2. Leaf size (visual estimate of length andwidth of leaf searched). This is probably
necessary mainly in areas where complexity of plant communities prevents quicktaxonomic identification of plant species(and therefore subsequent, more accurate
assessment of leaf size). Leaf buds should
also be distinguished, although these canbe “food” as well as substrate.
3. Top or Bottom. See Greenberg and Gradwohl(1980) and Greenberg (1984a) for theimportance ofdistinguishing leaf tops fromleaf bottoms. Greenberg and Gradwohl(1980) also found that a foliage-gleaning
tanager (Ducnis cayana) may inspect brown,
insect-damaged areas on leaves; therefore,
observers should be careful to record whensuch leaf sections are investigated.
Dead foliage. See Gradwohl and Greenberg(1982b). Remsen and Parker (1984). and Rosenberg’(this volume) for the importance ofdistinguishing live from dead leaves. Size ofleaf should also be recorded, as well as condition (curled, tattered, or entire; see Rosenberg, this volume) and general type (e.g., palm,
broadleaf, bamboo).
Bark or stem surfaces. Observers should notethat careful observations often reveal thatmany species generally thought to be foliagesearchers direct considerable proportions of
their attacks at branches and stems, such as
some species of vireos (Nolan and Wooldridge
1962; Root 1967; James 1976, 1979; Robinson and Holmes 1982; Airola and Barrett
1985), tanagers (Snow and Snow 1971, Islerand Isler 1987) wood-warblers (Morse 1967a,b, 1968; Lack and Lack 1972; Emlen 1977;
Greenberg 1984a), sylviids (Earl& 1983),
Hawaiian honeycreepers (Richards and Bock1973) shrikes (Earl& 1983) chats (Frith 1984),
Old World sallying flycatchers and drongos(Bell 1984), honeyeaters, whistlers, and babblers (Keast 1968, Thomas 1980, Wooller andCalver 198 l), and thornbills (Acunthizu;Bell1985b, Recher et al. 1987). When recording
use ofthis substrate category, the observer canrecord:1. Diameter (visual estimate)
2. “Angle” of branch (i.e., vertical, horizontal, or diagonal).
3. Upperor Lower side (for horizontal or diagonal branches). Some species may characteristically forage on the undersides oflimbs, such as the woodcreeper Xiphorhynthus lachrymosus(Willis 1983~).
4. Plant species,when possible, or plant type(see A.l. above). See Jackson (1979) andMorrison and With (1987) for examples of
the importance of tree species for woodpecker feeding-site selection.
5. Surfacetypeand texture(especially critical
where identification of plant species is notpossible). Examples include: (a) smoothgreen; (b) smooth bark; (c) rough bark (withBIOLOGY

D.

E.

F.
G.

G.

NO. 13perhaps a qualitative scale to indicate degree of corrugation); (d) seam between two
closely growing branches or between vineand supporting trunk (such seams appear
to be particularly favored foraging sites forsome dendrocolaptids; e.g., Hylexetustes
perrotii [Willis 1982f1); (e) lichen- or mosscovered (mossy branches are favored sites
for furnarids, dendrocolaptids,
severalbirds-of-paradise, and tanagers [Skutch
1969, 1981; Forshaw and Cooper 1979;
Parker and O’Neill
1980; Remsen 1984;
Parker et al. 1985; Remsen 19851); (f) hard,dead wood with bark removed; (g) soft,rotted dead wood (see Alatalo [ 19781, Cruzand Johnston 119791.Pettersson 119831.andMorrison et al. [ 1987b] for examples of theimportance of distinguishing live from deadbranches in bark-foraging birds; the furnariid Xenops minutus seems to be specialized on dead branches, especially thosethat have fallen but are caught up in the
canopy [Skutch 1969; T. A. Parker and
JVR, unpubl. data]); and (h) holes (favored
foraging sites for some dendrocolaptids[Willis 1982d, 4).
Ground
1. Surfacetype(e.g.,mud, bare soil, leaf-litter,
moss, gravel).
2. Distanceto nearestcover.
3. Slope(e.g.,flat, moderate slope, steep slope).
Rock
1. Size.
2. Surfacetype (e.g., smooth, rough, crevice).
3. Surface“angle” (top, bottom, side; verticalor diagonal slope).
Air
Flower (when identificationof plant unknown); as noted by Emlen (1977) it is often
difficult to distinguish whether some species
use flowers as sources of food (nectar feeding)or as substrates for searching for arthropods.
1. Corolla length.
2. Color.
3. Flower density (estimate no. flowers/unit
area; e.g., per 0.5 m*).
Miscellaneous. Almost every habitat will havesome substrates that do not fit into the above
scheme. For example, some species of birds
search pine cones (Morse 1967a, Ficken andFicken 1968, Emlen 1977, Moreno 1981), termite nests (Bell 1984), wasp nests (Willis
1982fj, spider webs (Young 197 1, Burtt et al.
1977, Douglass 1977, Waide and Hailman
1977. Bell 1984. Brooks 1986. Tiebout 1986.
Parrish 1988, Petit and Petit 1988) dung (An:derson and Merritt 1977), and even the skinof other vertebrates (Rice and Mockford 1954,
Orians 1983, Isenhart and DeSante 1985 andreferences therein, Robinson 1988). For fmiteating birds, we do not record a substrate perse, but note certain characteristics of the fruit
under “food taken” (see next section).

Although the number of parameters to be recordedin this classification of foraging maneuvers and sub-

CLASSIFICATION

OF BEHAVIOR--Remsen

and Robinson

157

FIGURE 2. Sample foraging data transcribed from microcassetteto field notes. Codes: “HT” = height above
ground, “DC” = distance-to-canopyabove bird, “FD” = foliage density, “DL” = dead leaf, and “vs” = visual
search. Vertical brackets near left margin group consecutive observationson same individual. The thin lines
under the “Substrate” column record branch “angles,” and tiny “x” marks record position of bird with respect
to branch. (Height variables are in feet, and substratevariables are in inches.)

strate characteristics may seem complex and overwhelming, the advent of microcassettetape-recorders
facilitates recording such volumes of data in the field.
Also, transcription of the data can be simplified byusing codesand symbols (Fig. 2).
FOOD TAKEN
Data on diets are useful for virtually every kind of
foraging study. Differences in food taken may provide
information on niches, morphology (principally of thebill), and energetics.Unfortunately, dietary data areusually difficult to obtain in the field, especially for
insectivores.

For many speciesthat eat small insects,it can evenbe difficult to determine whether or not a prey item
was capturedat the end of an attack. For thesereasons,most field studiesof insectivoresinclude only limited
data on prey. Variables measured include prey size(usuallyin relation to bill length, but seeBayer [19851
and Goss-Custardet al. [ 19871for cautions)and preytype (for large prey items such as caterpillars and orthopterans).Some authors (e.g., Greenberg 1984a) recorded each time that a bird wiped its bill after a prey
attack as an index of success.Reasonablyaccurateestimates of capturerates can be obtained for large prey,such as orthopterans that require extensive handling

158

STUDIESIN AVIAN

before they are eaten (Robinson 1986). Many neotropical insectivores evidently obtain most of their energy from large katydids (Orthoptera: Tettigoniidae)
and have bills adapted specifically to handle them(Greenberg 198 la). Most temperate-zone insectivores,on the other hand, have smaller bills, presumably
adapted for the smaller arthropods or less agile larvae
available during the breeding season. Because large fooditems have more biomass than small items, we thinkthat food size should always be recorded where feasible.
For frugivores, the most important variable is theplant species. Secondary variables include the color (asa measure of ripeness), size (especially if the plant species
is unknown), and shape of the fruit. For nectarivores,
the plant species is again the primary variable of interest. If this is unknown, then color, shape, and corolla
length should be recorded.
Data obtained from stomach samples are discussed
elsewhere in this volume (Rosenberg and Cooper). Herewe wish only to emphasize that stomach samples canbe very useful when they reveal major ordinal levelsof dietary differences among species being compared.
Sherry (1984), for example, showed that species thatare generally similar in size and foraging behavior candiffer strikingly in their diets. Dietary analyses of Least
Flycatchers (Empidonax minimus) and American
Redstarts, which are strikingly similar in many aspectsof their foraging behavior and foraging-site selection(Sherry 1979), revealed surprisingly little overlap (Robinson and Holmes 1982). In this case, knowledge ofdiet from stomach samples (redstarts catch manyneteropteran leafhoppers) provided information on thefunctional significance of the “flush-chase” attack maneuver described previously.
Data from stomach samples should, however, betreated with caution. Because prey items in stomach
samples can usually only be identified to the level oforder or family, the categories are crude. It is quitepossible that two species that eat the same orders, families, or even genera of insects could overlap very little
in other aspects of their foraging behavior, particularly
substrate use. Information on diet in the absence ofdata on other components of foraging (e.g., Wiens andRotenberry 1979) therefore could be misleading.

FOOD-HANDLINGTECHNIQUES

Once food is “captured,” it may be eaten, delivered
to offspring or mate, stored (cached), or rejected. We
here consider only the techniques associated with thefirst of these options. The way that food is handled isimportant because (1) food-handling time must be considered in the cost : benefit ratio of any food type (e.g.,
Sherry and McDade 1982) (2) it is a factor in studies
ofadaptive morphology (e.g., Sherry and McDade 1982,
Moermond and Denslow 1985, Foster 1987) and (3)it has important implications for the study of plantfrugivore interactions (Howe and Smallwood 1982,
Moermond and Denslow 1983, Levey 1987b). Foodhandling techniques, however, have been largely ignored in studies of arthropod-foraging behavior (forexception, see Sherry and McDade 1982). Fortunately,
the detailed descriptions by some observers (e.g., E. 0.
Willis and A. F. Skutch) have revealed the distinctive
behaviors associated with handling of various foodtypes. The lack of data on food-handling techniques,

BIOLOGY

NO.

13

particularly in insectivores, prevents an evaluation of
their relative frequencies of use. In addition to quantifying the time taken to manipulate food before swallowing, we recommend the following terms to describe
techniques that we feel are appropriate for field observations of landbirds:
1 Engulj?to capture and swallow in one continuous
motion, without being held by the bill.
2 Gulp (after Moermond and Denslow 1985): toswallow upon capture without any noticeable manipulation other than being held briefly by the bill.
3 Snap: to pinch momentarily, usually between tips
of mandibles and usually to kill prey before further
handling.
4 Mash (after Moermond and Denslow 1985): tosqueeze or move around between the mandibles
before swallowing (apparently to kill prey or remove undesirable portions, such as wings, legs,
shells, and husks); sometimes, juices or pulp are
squeezed out of the food and solid portions discarded (Moermond and Denslow 1985, Foster
1987). This category almost certainly lumps distinct types ofmandibulation that could be revealedby analysis of high-speed photography of foodhandling.
5. Shake: to shake food item violently (to remove
undesirable portions).
6. Beat: to beat food item against hard substrate (asin above, to kill or remove undesirable portions).
Many small insectivorous birds typically beat insects against branches in a diagonally downwardfacing position (e.g., Root 1967).
7. Rub: to rub food along substrate (usually to remove distasteful substances or undesirable portions such as hairs and stingers [Sherry and McDade
19821).
8. Jab: to peck food item with bill tip (to kill it oropen it), usually while clasped with feet.
9. Tear: to eviscerate or dissect food item into smaller pieces, usually while the food is clasped by one
or both feet.
10. Bite: to bite and remove a section of food item
(after Foster 1987). This technique applies as far
as we know only to frugivores that take bites fromfruit too large to swallow whole.
11. Juggle:to reposition food item, sometimes by tossing into air and catching it (to allow or facilitate
swallowing; many species juggle prey to maneuver
it into a head-first position before swallowing).
12. Clasp:to hold food item with feet.
13. Anchor:to immobilize food item by fixing it to
substrate, such as by impaling with sharp objects
or by wedging food item into crack.
14. Drink: intake of liquid food, such as fruit juices
and nectar.
In practice, we have found that in the field, we havetime to note only those food-handling behaviors thatare not “gulping,” which seems to be the predominantfood-handling technique in most insectivorous andfrugivorous birds, with the notation that all “blank”
records refer to gulping. Our scheme leaves out certain
techniques that are presumably very rare, such as
scraping (to remove fruit pulp in snake-like jaw motion; Schaeffer 1953), dropping (to break open), soaking, and drowning.

CLASSIFICATIONANALYSESOF FORAGING

OF BEHAVIOR--Remsen

DATA

This classification system contains many finely
subdivided categories. Although too many cancreate problems (e.g., small or empty data cells)
for statistical analyses, we think that fine subdivisions are preferable during the data-gathering stage. Their retention allows maximum data
resolution, which in turn, even if sample sizes
are too small for statistical analysis, might generate insights that can be developed to answer
specific questions in subsequent studies. Here we
provide examples of how categories might be
combined or subdivided.
I. Ecomorphoiogicalstudies.Fine subdivisionsof attack methods, foraging substrate, andsearching behavior are most likely to be usefulin studies of adaptive morphology. Fitzpatrick(1985) for example, showed that many aspectsof bill and wing shape were strongly associatedwith the details of aerial attack methods (see Table 1) and substrate in tyrannids, whereas leg
morphology was more closely related to searching movements and perch types. Fitzpatrick’s(1985) classification system of foraging methods,
therefore, combined searching movements, perchtypes, substrate type, and attack method in an
attempt to include all of the variables that affectflycatcher ecomorphology. The bill morphologies of bark-foraging birds are also affected by
the methods used to manipulate the substrate toattack concealed food. The finer subdivisions ofnear-perch maneuvers (see Table 1) also may berelated to leg and foot morphology (Partridge
1976a, Leisler and Winkler 1985). The bill shapesof frugivores and some insectivores may also be
associated with particular kinds of food (Greenberg 198 1, Moermond and Denslow 1985, Foster
1987).
II. Community-levelstudies.Community-levelstudies probably require the least finely subdivided categories. Communities in wooded habitats are likely to include birds that use most of
the attack methods described in Table 1. If eachmethod were to be broken down by substrate,
the resulting data matrix would be prohibitively
large and would contain many zero values. For
this reason, most studies that seek to identify
guilds use only a few general attack categories(e.g., Holmes et al. 1979b) or use only data on
foraging site (Anderson and Shugart 1974).
Holmes et al. (1979b), for example, divided theattack methods of birds in a northern hardwoods
forest into “gleans” (lumping all “near-perch”
maneuvers in Table l), “hovers” (all sallies tosubstrates other than air in Table 1), “probes”(including all subsurface maneuvers in Table l),
and “hawks” (all sallies directed at flying preyin Table 1). Each of these attack methods wasthen combined with a foraging site. The resulting

and Robinson

159

analysis showed that such variables as substrate
and tree species were more important in assigning species to guilds than attack methods. By
contrast, in a similar analysis of an Australian
bird community, which added categories forflush-chase and manipulative
prey-attacks,
Holmes and Recher (1986a) found that attack
methods were also important. The different guild
structures in the two areas may have been influenced, therefore, by their differing classification
systems. In general, we recommend that manipulative attack-methods be distinguished frommethods in which food is simply plucked fromsurfaces or the air in studies of entire communities.
III. Single-guild studies (taxonomic guilds,
sense Terborgh and Robinson 1986). Studies that
focus on ecologically similar species should benefit from fine subdivisions of substrates and attack methods. The members of a guild are only
likely to use a subset of the attack methods shownin Table 1, which should simplify the matrices
and allow finer subdivisions. Rosenberg (thisvolume), for example, included data on the sizeand shape of dead leaves searched, and Greenberg’s (1987a, b) study of a dead-leaf forager included data on searching postures similar to thesubdivisions of near-perch attacks shown in Table 1. Conner’s (1980, 198 1) studies of bark foragers showed the importance of different methods of manipulating substrates in distinguishingamong species. Fitzpatrick (1980, 198 1) showed
the different ways that syntopic tyrannids differ
in the subtle details of how they sally to catchprey.
IV. Foraging modes (sensuHuey and Pianka
198 1) or adaptive syndromes (sensu Eckhardt
1979). Studies of foraging modes seek to identify
suites of intercorrelated foraging variables. Many
researchers have shown that the rates and lengthsof searching movements are associated with thelengths and kinds of attack methods (e.g., Williamson 1971; Eckhardt 1979; Fitzpatrick 1981;
Robinson and Holmes 1982; Holmes and Recher
1986b; Holmes and Robinson 1988; see also
Moermond 1979a and Huey and Pianka 1981
for similar analyses of foraging in lizards). In
general, birds that move short distances between
perches also obtain food on nearby substrates.
Similarly, species that fly long distances between
perches also search and attack over long distances. Studies of adaptive syndromes therefore
include detailed data on searching movements(including rates and lengths), attack tactics (including lengths of attacks), and the use of special
foraging tactics such as tail-fanning. Table 2 gives
examples of adaptive syndromes or foraging
modes that have been identified in New World
insectivorous birds (modified from Eckhardt[ 19791, Fitzpatrick [198 11, and Robinson andSTUDIES

160
TABLE 2.

IN AVIAN

NO. 13

ADAPTIVESYNDROMES OR FORAGING MODESOF INSECTIVOROUS
BIRDS
ForagingmodeOpen perch or passive searching
Medium-distance searching
Near-surface searching
Flush-Chasing
Manipulative

Associatedprey-attacking
maneuvers

Searchmovements

Infrequent, long flights
Frequent medium-length flights andbouts of hopping
Frequent hops and short flights
Conspicuous,frequent flights andhops, wing and tail flicking
Short periods of movement between
long periods at the substrate

Holmes [ 19821). Whether these relationships haveglobal generality remains to be determined.
V. Energeticsand optimalforaging. Studies ofenergetics or optimal foraging primarily use dataon time intervals between movements and foodcapture rates. Robinson (1986) for example,
measured intervals between flights of at least one
meter as an index of foraging speed and preycapture rate, and prey size as an index of foraging
success.Energetic studies therefore require long,
timed sequences on individual birds in which
the length and kinds of every movement are recorded. As already noted, food-handling time isa critical variable in studies of optimal diet selection (e.g., Sherry and McDade 1982).
CLOSINGBIOLOGY

REMARKS

Although portions of our classification scheme
have been used by us or other researchers formany years, other portions were novelties generated by rethinking the underlying logic of ear-Long sallies
Sallies and near-perch gleans
Near-perch maneuvers, probes
Flush-chases
Flake, peck, tear, hammer,
scratch,chisellier versions or by incorporating suggestionsfrom
other researchers. We regard this scheme as afirst step towards standardization of the organization and vocabulary of studies of foraging
behavior of birds. We anticipate that it will be
modified as it is tested and refined by us and, wehope, other researchers.
ACKNOWLEDGMENTS
We thank C. L. Cummins, R. Greenberg, R. T.
Holmes, T. C. Moermond, M. L. Morrison, T. A. Parker, K. V. Rosenberg,and T. S. Schulenbergfor valuable comments on the manuscript or portions thereof,
and Donna L. Dittmann for preparation of Figure 1.
The authors’ fieldwork, critical for the formulation of
the ideas and proposed scheme presented here, hasbeen supported generously by (for JVR) John S.
McIlhenny, H. Irving and Laura Schweppe, BabetteOdom, and the National Geographic Society, and (forSKR) the Chapman Fund of the American Museumof Natural History, the National ScienceFoundation,and the Society of Sigma Xi.