Download DIET SELECTION IN AMAZONIAN ANTWRENS: CONSEQUENCES

The Auk 110(2):361-375, 1993
DIET
SELECTION
IN AMAZONIAN
ANTWRENS:
CONSEQUENCES OF SUBSTRATE SPECIALIZATION
KENNETH
V. ROSENBERG 1
Museumof NaturalScience
andDepartment
of ZoologyandPhysiology,
Louisiana
StateUniversity,BatonRouge,Louisiana
70803,USA
ABSTRACT.--Iused an observationaland experimental approach to investigate the dietary
consequences
of substratespecializationin sixspeciesof Amazonianantwrens(Myrmotherula).
Three species(leucophthalma,
haematonota,
and ornata)foragedexclusivelyat curleddeadleaves
suspendedabove ground, axillarisand longipennis
foraged on live foliage, and hauxwelliwas
a substrategeneralist,feeding at both live and dead foliage.Diet compositionof all species
wasqualitatively similar, with soft-bodiedorthopteransconsistentlythe mostimportant prey
type. Dead-leafspecialiststook other prey roughly in proportion to their availability in dead
leaves,whereasdietsof live-leaf foragersdifferedgreatlyfrom prey availableon live foliage.
Dead-leaf specialistsalso ate larger prey and especiallylarger orthopteransthan did other
antwrens. Substrategeneralization in hauxwelliwas associatedwith higher diet breadth and
greaterheterogeneityamong individuals,comparedwith substrate-restricted
foragers.Diet
breadthwasnegativelycorrelatedwith prey sizeacrossall six species.When testedin outdoor
cages,live-leaf foraging and generalistspeciesshowedlittle interest in dead- or live-leaf
substrates,whereasall dead-leafersrepeatedly inspectedand manipulated dead and curled
leavesin the absenceof food. All foraging groupsshoweda similar degree of selectivityof
prey types in feeding trials. Dead-leaf specialistsdid not differ from other speciesin their
preferencefor orthopteransof different colors,although specialistswere better able to catch
and handle the largest katydids (>30 mm). Individual hauxwelli(the generalist) showed
elevatedlevelsof explorationat deadleaveswith food reinforcement,suggestingshort-term
plasticityin searchbehavior.I concludethat substratespecializationin thesebirds involves
fundamental differencesin searchbehavior, but is not accompaniedby equivalent changes
in prey selectivityor preference.Dead-leaf specialistssearchfor suitablesubstratesand then
inspectthem for hidden prey, taking prey roughly in proportionto their availability.In
contrastlive-leaf foragerssearchdirectly for prey and selectsuitableitems from the wider
array of arthropodsavailableon live foliage. Substrate-restricted
foragingmay reducediet
breadthandpromotedietstereotypyin bothgroups,whereasthe singlemostimportantfactor
promotingspecialization
on deadleavesmaybe the predictableabundance
of relativelylarge
orthopterans.Received
25 November1991,accepted
27 May 1992.
DIETSELECTION
in birds may be influencedby predator-prey interactions were important in
morphology,foraging behavior, microhabitat shapingforagingniches.In this study,I invesselection, innate food preferences, and avail- tigated the effectof foraging specializationon
ability of food resources.Studiesrelating avian diet selectionin an assemblageof morphologdiets to specific behaviors or microhabitats, ically and ecologicallysimilarantwrens(Myrhowever, have been few. For an assemblageof motherulaspp.) that inhabit the understory of
insectivorous birds in a northern deciduous forprimary Amazonianrain forest.
est, Robinson and Holmes (1982) concluded that
Foragingspecializationis thoughtto promote
in complexcommunities,especially
dietswere constrainedby species-specific
search coexistence
tactics,aswell asthe distribution of prey among amongtropicalforestbirds (Orians1969,Terforaging substrates.In one of the only studies borgh1980,Remsen1985).The extentto which
resultsin dietarydifferences
that considereddiets of tropical insectivorous suchspecialization
isnotwell known.If specialized
birds,Sherry(1984)alsoconcluded
thatspecific amongspecies
behaviorsrestrict a bird's accessto prey or limit
itsexposureto certainpreytypes,coadaptations
• Presentaddress:Laboratoryof MolecularSystem- between suchpredatorsand their prey may poatics,Museum SupportCenter, NMNH, Smithsonian tentially evolve,possiblyleadingto innateprey
preferences.
If, alternatively,specializedbeInstitution,Washington,D.C. 20560,USA.
361
362
KENNETH
V. ROSENBERG
[Auk,Vol. 110
haviors serve to partition foraging spacewith- 1988,and 1989at the TambopataReserve,Department
out subsequentsegregationof diet, the role of of Madre de Dios, southeastern Peru (12ø50'S,69ø17'W;
resource-basedinteractionsin promoting spe- 290 m). This is an area of tall, primary Amazonian
rain forestdescribedfurther by Erwin (1985) and Rosenberg(1990b).I made additional observationsdurThe antwrensI studiedhave been the subject
ing June through August 1986 in similar rain forest
of severalecologicalinvestigations(Wiley 1971, near Cobija,Departmentof Pando,northwesternBo1980, Pearson 1977, Jones 1978) that have re- livia, about 200 km north-northeast of Tambopata.
ported subtle differences in behavior and for- Also at the Pando site,birds were collectedfor dietary
aging heights thought to allow coexistence analysisaspart of a generalavifaunalsurveyby the
among species.These speciesrange in size from Louisiana State University Museum of Natural Sci7 to 10 g, and arevirtually identicalin bill length ence (LSUMNS; Parker and Remsen 1987). Supplecialization
is less clear.
(15-16 mm). Most antwrensare typical gleaners
of live foliage; however, several speciesare
highly specialized searchersof curled dead
leaves suspendedabove the ground (Remsen
and Parker1984,Gradwohland Greenberg1984,
Rosenberg 1990a, b). Previous investigators
(Gradwohl and Greenberg 1982, 1984, Rosenberg 1990a, b) concluded that dead-leaf spe-
mental
diet data came from birds collected
at a few
randomlycomparedwith that available;and (3)
were exposedto different prey resourcesfrom
antwrens that search live foliage. Therefore,
substratespecialization may be important in
promoting resourcepartitioning in these species, through dietary differences.Potential for
and perch type. My terminologyfor describingforaging behavior closely follows that of Remsenand
othersitesin southwesternAmazonia,especiallynear
Abujao,Departmentof Ucayali,Peru(LSUMNS stomach-contents collection).
! observedforaging antwrensby following indi-
viduals in mixed-speciesflocks, encountered opportunistically along forest trails. To minimize consecutive observations of individuals, I rotated my
attentionamongseveralspeciesin the sameflock. For
cialist antwrens: (1) searched dead leaves in 98 eachbird I recordedspecies,sex,foragingheight (esto 99% of their foraging attempts;(2) selected timated to nearest 1 m), method (glean, hover, etc.),
foraging substrates(leaf types)and prey non- substrate(including specific leaf surface and size),
interactionsbetween specialistand nonspecialist speciesis enhanced becauseboth typically
join the samemixed-speciesforaging flocksand
mayfeed side-by-sidein a group-defendedterritory (Munn and Terborgh 1979, Munn 1985).
My study combined observationaland experimental approachesto investigate the consequencesof dead-leafsubstratespecialization
for diet selection.I first comparedthe behavior
and diets of wild antwrens,asking:(1) do deadleaf specialistspeciesdiffer in diet composition
and prey sizefrom live-leaf foragingand generalist species;and (2) are prey types selected
accordingto their availability in nature?Then,
using a seriesof outdoor cage experimentson
wild-caughtantwrens,I asked:(1) do thesespecies differ in their natural tendency to search
or manipulate particular foraging substrates
(deadversuslive foliage);(2) are thesetendenciesinfluencedby food availability;and (3) do
preferencesfor prey types under controlled
conditionsmatch these species'natural diets?
STUDY AREAS AND METHODS
Behavioralobservationsand experimental studies
of antwrens were conducted over 10 months in 1987,
Robinson (1990).
Diets were assessedfrom stomach contents preserved in 70% ethanol as soon as possible after collection.Sampleswere sortedand identified to lowest
taxonomiclevel possibleunder a 6 x -25 x dissecting
microscope.Minimum number of prey items in each
categorywas determined from diagnosticfragments,
such as mandibles (Orthoptera, larvae), fangs (spiders),heads,or wings (beetles,Heteroptera).I determined the proportionsof prey categoriesin each individual stomach and then averaged these across
individuals to determine the diet compositionof each
species(i.e. sampleswere not pooled). I compared
diets among speciesusing G-tests(Sokal and Rohlf
1981:704)basedon the frequencydistributionsof prey
categories,
adjustedto reflectthe averageproportions
of each prey categoryfor each species.For example,
the adjustedfrequencyof spidersfor a speciesequaled
the averageproportionof spidersfor that speciesmultiplied by the total number of prey items in the sampie. In somecases,stomach-contents
datamay not be
appropriatefor such statisticalanalysesbecauseof
potential nonindependence (i.e. pseudoreplication)
amongprey items in individual stomachs(Hurlbert
1984). However, becauseantwrens forage methodically and may searcha variety of substrates
between
successfulprey captures,and becauseidentical prey
types rarely appear more than once in any stomach,
I believe it is appropriate to treat prey items as independent.
Prey sizewasestimatedfrom the size of characteristic fragmentsusing regressionequationsin Calver
and Wooller (1982) and Diaz and Diaz (1990), or determined from voucher specimensfrom this study.
April 1993]
DietSelection
in Amazonian
Antwrens
363
Prey-sizedistributionswere comparedamongspecies maximum of 10 min, although I sometimesleft unusing Kolmogorov-Smirnov(K-S) tests (Sokal and eatenprey in the cageduring subsequenttrials to see
Rohlf 1981:714).
if initially rejectedarthropodswere eventually eaten.
Diet heterogeneity
wasassessed
in twoways.Over- I scoredeach responseon a subjectivebut unambigall dietary breadth for each specieswas computedas uousscale(Table 1), rangingfrom completelyignored
(0) to eagerly and quickly consumed(4). To assurea
B = 1/2 p,2,
(1)
wide array of possibleprey offerings, my assistant
where p,is the proportionof categoryi in the sample and I captured arthropods using sweep nets, by
(Levins1968).I usedthe averageproportionsof nine searchinglive anddeadleaves,andby searchingalong
prey categoriesto calculatethis measure.Also, as a trails at night with lights. Somefrequently usedprey
measureof stereotypyamong individual stomachsin
(e.g. katydids)were kept for severaldays in nearby
eachsample,I calculatedpopulationdietary hetero- enclosures.Still, the range of prey offered to each
geneity (PDH) as the G-statistic(from matrix of nine
bird waslimited by the day's"catch,"and it wasoften
prey categoriesfor n stomachs)divided by degreesof not possibleto replicate some prey types acrossall
freedom for that sample (Sherry 1984). This latter individuals.
measureis thought to reflect evolutionarily conUsually,after severalsuccessful
feedings,the bird
strainedaspectsof diet specializationrather than eco- showedsignsof searchingfor food in the cagebelogicalresponseto resourceavailability(Sherry1990). tweentrials.At this point I begana seriesof substrate
Prey availability was estimated at Tambopataby trials by attachinga dead leaf and a live leaf (or sprig
searchingindividual dead and live leavesfor arthro- of leaves) to the percheswith wooden clothespins,
pods, as describedin Rosenberg(1990a,b). Samples without associatedfood. The positionsof dead and
of 1,918 dead leaves and 3,155 live leaves, all from
live
substrates
were
switched
in
successive
trials.
within 3 m aboveground,were usedin this analysis. Again, I observed,timed, and recordedeachresponse,
I comparedfrequenciesof prey types in bird diets and scoredtheseon an unambiguousscaleof behavwith availabilitysamplesusingG-testsbasedon nine iors (Table 1), ranging from ignored (0) to repeated
prey categoriesequally detectablein leaf and stomach physicalmanipulation of the leaves(5). I then altersamples.A significantdifferencein the distribution natedboutsof substrateand feeding trials until late
of prey types used and available was consideredevidence of selectivityby that species.
afternoon, when the bird was released(usually about
1600). If time permitted, I combined substratesand
Antwrens were capturedfor feeding experiments prey in the same trial (i.e. prey were placed on or
usingmist netsplacedin areaswhere flocksforaged.
My initial attemptsto keep birds in captivity for periods greater than one day were unsuccessful;
therefore, prolongedperiodsof adjustmentto captivityor
repeatedtestingof individual birds was not possible.
For this reason,only birds capturedbefore 1000EST
insideleaves)to observechangesin behavioror capture efficiencyby birds feeding on "normal" versus
"abnormal" substrates;for example, could a live-foliage speciescapture prey hidden in dead leaves, or
could a dead-leaf specialistfind cryptic prey on live
leaves?
were used as subjects,and only one individual could
be used per day. Capturedbirds were immediately
placedin the cageand allowed to adjustfor about i
h. The cageconsistedof a frameof white plasticPVC
tubing (0.5 x 0.5 x 0.5 m) coveredwith fitted mosquito netting and equippedwith a closableopening
on one side. Two diagonally oriented dead branches
servedas perches,and the cage was placed in the
shadeon the forestfloor. Through trial and error, I
determined
that this small-sized
enclosure
worked
RESULTS
FIELD OBSERVATIONS
Foragingbehavior.--Amongthe antwren species (Myrmotherula) I studied: leucophthalma
(White-eyed Antwren), haematonota
(Stipplethroated Antwren) and ornata (Ornate Ant-
best;birds were lessdistractedand more quickly be- wren) useddeadleavesalmostexclusively;axilcamecalm and acceptedfood.
laris (White-flanked Antwren) and longipennis
After the initial waiting period, I placedseveral (Long-winged Antwren) used live foliage of
food items(usuallysmall katydids)on the floor of the various types; and hauxwelli (Plain-throated
cageand again left the bird undisturbed for about 30
min (timesvariedamongsubjects).
If after thisperiod
theseprey were readily consumed,I began a series
of feeding trials. For eachtrial I placeda previously
identified and measuredarthropodon the cagefloor
and returnedto a spotroughly 10 m from the cage
and partiallyconcealed
by foliage.I then closelyobservedthe bird'sresponse
using10x binoculars,timed
eachbehaviorwith a stopwatch,and recordedthese
continuouslyonto a microcassette.
Eachtrial lasteda
Antwren) wasa substrategeneralist,searching
dead and live leaves as well as stems, ferns, and
moss (Fig. 1). Myrmotherulahaematonotaoc-
curredonly at the Pandosite,in uplandforest,
where it joined mixed-species
foragingflocks
with axillarisand longipennis.
All speciesexcept
haernatonota
occurredat Tambopata,
andall species except hauxwelliregularly joined mixedspeciesflocks.
364
KENNETHV. ROSENBERG
TABLE1. Responsescoring systemused for captive
antwrens offered a variety of substratesand prey
types.
Score
hauxwelliforagedmuch lower than the other
species(Fig. 2) and, typically,perchedon thin,
vertical stems(84% of observations).I never observedthis specieson the ground, however, in
contrast with some other published accounts
(e.g. Pearson1977).
Definition
Substrates
0
1
2
Ignored.
Briefly looked at from short distance.
Closely inspected(but did not touch).
3
Touched
4
5
Manipulated or probed inside.
Repeatedmanipulation, probing, or tearing.
0
1
2
3
4
Prey types
Ignored.
Initially attacked but rejected (did not eat).
Initially rejectedbut eventually eaten.
Tentative, hesitant, but readily eaten.
Very quickly attackedand eaten.
surface with
[Auk, Vol. 110
Diet composition
andpreyavailability.--Thediets of all six specieswere dominated(63-92%)
bybeetles,
orthopterans
(includingroaches),
and
spiders(Fig. 3). Subtledifferencesin the proportionsof prey categories,however,resulted
in significantheterogeneityamongspecies(G
bill.
= 166.2, df = 40, P < 0.001). Pairwise compar-
isons,controllinga-level for multiple tests(Sokal and Rohlf 1981:721),revealed that the diet
compositionsof ornata,axillaris,longipennis,
and
hauxwellidid not differ significantly(P > 0.02).
The diet of ornata also did not differ from leu-
In both the dead-leaf and live-leaf foragers,
the two co-occurringspeciesdiffered slightly,
but significantly,in averageforaging height
(Fig. 2; t = 9.6 for dead-leafforagers,4.0 for
live-leaf foragers,P < 0.001);haematonota
foraged lower at Pandothan did the other dead-
cophthalma.
However, haematonota
and leucophthalmadid differ in diet from the generalist
and live-leaf-foraging species(P < 0.001). In
general, the dead-leaf-specialist
speciesate a
higherproportionof orthopteransand roaches,
whereasthe two live-leaf foragersate more lar-
vae. The generalisthauxwellishowedthe most
leaf-foraging speciesat Tambopata(œ= 1.8 m; varied diet, with the highestproportionsof ants,
not shown).Myrmotherulalongipennis
alsoused flies, and wasps,as well as the fewest orthopaerial maneuvers(e.g.hovering,sallying)more terans.
often than axillaris(73 vs. 58%). Myrmotherula
Prey availability in dead leaves consisted
1,0-
[]
•
,0
(•'
ß Stem
0.6
[]
0
•
0
Other
0.8
Palm/fern
[] Liveleaf(bottom)
0.4
[]
0
Liveleaf (top)
[] Liveleaf
Q-
(undifferentiated)
,O 0.2
Q-
ß Deadleaf
0.0
MHAEM
MLEUC
MORN
MHAUX
MAXIL
MLONG
(81)
(941)
(538)
(69)
(248)
(254)
Species
Fig. 1. Foragingsubstrate
useby five species
of antwrensof the genusMyrmotherula:
(MLEUC)leucophthalma;
(MORN)ornata;
(MHAUX)hauxwelli;
(MAXIL)axillaris;
(MLONG)longipennis.
Numberof observations in parentheses.
April 1993]
DietSelection
inAmazonian
Antwrens
20
365
green on live foliage. All orthopterans in dead
leaves were brown,
whereas 21% of those on
live leaves were brown and 67% were green.
Average size of all arthropods in dead leaves
was significantly larger than those on live foliage (6.5 vs. 5.3 mm), aswasthe sizeof available
orthopterans(12.9 vs. 8.0 mm). Over 50%of the
orthopterans in dead leaves were greater than
10 mm, comparedwith 22% on live leaves.Thus,
birds foraging on live and dead leaves are exposedto different proportionsof prey types,as
well as prey of different colors and size distributions.
Compared with prey availability, all species
selectedorthopterans(Fig. 4) and for all species,
(1042)
(578)
(124)
(465)
(312)
diet differed significantly from proportionsrepSpecies
resentedin available prey (G-tests,P < 0.001).
Fig. 2. Averageforagingheightsof five speciesof The dead-leaf specialiststook other prey types
antwrens. Vertical bars indicate + 1 SD; vertical lines
roughly in proportion (+10%) to their availindicaterange.Number of observationsin parenthe- ability in deadleaves.The two live-leaf foragers
ses.Speciescodesfrom Figure 1.
exhibited greater selectivity, eating more beetles and larvae than expected,and many fewer
mostly (75%) of spiders, roaches,beetles, and ants, flies, and wasps. The diet of hauxwellidiforthopterans,whereasthesemade up only 35% fered from arthropoddistributionson both dead
of the arthropods on live foliage (Fig. 3). In and live leaves, but was closest to that on dead
contrast,one-half of the prey on live leaveswere leaves.
ants, flies, and wasps. In addition, 83% of arThe three dead-leaf specialistsexhibited the
thropods in dead leaves were brown and 4% narrowest dietary niche breadths (Table 2),
were green, comparedwith 38%brown and 18% whereas the generalist hauxwelli showed the
MLEUC MdRN MH•UX MAXIL ML•NG
[]
Other
[]
Fly/wasp
[]
Larva
0.8'
0.6'
[] Ant
[]
Heteroptera
0,4'
[]
Beetle
[]
Spider
0.2'
[] Roach
[]
Orlhoptera
0.0
MHEAM MLEUC
t3/149
18/181
MORN
MHAUX
MAXIL
MLONG
DL
LL
7/92
9/103
21/269
12/163
1039
396
Species
Fig.3. Diet composition
of fivespecies
of antwrens(species
codesfromFig. 1)andcomposition
of available
prey on dead(DL) and live leaves(LL). Samplesizesfor birdsare numberof stomachs/number
of prey items,
and for leavesare number of arthropodssampled.
366
KENNETH
V. ROSENBERG
50'
MHAEM
versus
deed leaves
[Auk,Vol. 110
30-
MLEUC
versus
dead
leaves
40'
30'
20'
10:
-10:__
-20:
-20:
-30
MORN
versus
dead
leaves
30'
20
20'
lO
10
MHAUX
versus
live leaves
MLONG
versus
live leaves
0
-•o-
-10
-20'
-20
-30
MAXIL
301
versus
live leaves
301
20
10
o]
-10
-10
-20
-20
-30
•30
•
o
•
o
Fig. 4. Comparisonof diet and prey availability for five speciesof antwrens. Horizontal line (at "0")
indicatesuseequal to availability; barsabovehorizontal indicateselectionand barsbelow horizontal indicate
avoidanceof prey. Speciescodesfrom Figure I.
April 1993]
DietSelection
in Amazonian
Antwrens
367
T^BI,E 2. Dietary characteristics
of six Amazonian antwrens. Prey sizesare • ñ 1 SD (number of prey items
in parentheses).
Myromotherula
Diet breadth
Population
dietary
heterogeneity
haematonota
leucophthalma
ornata
axillaris
longipennis
hauxwelli
2.70
4.08
4.93
5.15
5.00
6.18
0.77
0.95
0.98
1.00
0.92
2.15'*
Prey size (mm)
13.3 ñ
12.6 ñ
11.3 ñ
8.8 ñ
9.3 ñ
7.6 ñ
5.7 (139)
6.6 (119)
6.0 (70)
4.1 (169)
5.0 (105)
6.6 (65)
Orthoptera
size (mm)
15.7 ñ
17.6 ñ
16.1 ñ
12.6 ñ
13.5 ñ
12.6 ñ
5.1 (95)
6.0 (56)
5.6 (28)
3.5 (65)
4.6 (47)
3.6 (17)
**, P < 0.001, (G-test).
highestdiet diversity.In termsof heterogeneity
among individuals (PDH), dead- and live-leaf
foragershad similarly uniform diets.Myrmotherula hauxwellishowed greater heterogeneity,
and only this value was associatedwith a significant G-statistic(P < 0.001). Population dietary heterogeneity for samplesfrom a single
site varied from 0.50 for leucophthalmafrom
Abujao, Peru (n = 5) to 3.07 for hauxwellifrom
Tambopata,Peru (n = 4). In no specieswas PDH
for the pooled samplegreater than that for individual sites,suggestingthat geographicvariation did not contribute to overall dietary heterogeneity in these species.
Estimatesof averageprey size were larger in
the dead-leaf-specialistthan in the live-leaf foragersor the generalist(Table2); differenceswere
significantfor all comparisonsexceptornataversus longipennis(K-S tests, P < 0.05). All three
dead-leafspecialists
alsoate significantlylarger
orthopterans(as estimated from mandible size)
than generalist or live-leaf-foraging antwrens
(K-S tests, P < 0.05). The clearest distinction
between thesegroupswas in their predation on
large orthopterans (> 17 mm); these comprised
19 to 24% of all prey consumedby the deadleaf specialistsversusonly 2 to 5% of prey in
the other species.Acrossall six species,average
prey sizewashighly, negativelycorrelatedwith
diet breadth (r = -0.912,
Substrateresponse.--Theclearest distinction
between specieswas in their responseto deadand live-leaf substrates, without associated food
(Fig. 5). The two live-leaf-foraging speciesand
the generalist showed little interest in either
leaf type, scoringbetween 1.4 and 2.1 on my
scale.Typically,individualsof thesespeciesinspecteda leaf briefly from severalcentimeters
away and then ignored it for the remainderof
the trial. They rarely touched a leaf with the
bill (10 of 43 trials), and in only 3 of 43 trials
did an individual
look inside a curled
dead leaf
for potential prey.
In sharp contrast, all individuals of the two
dead-leaf-specialistspecies exhibited typical
dead-leaf-searchingbehavior, repeatedlyprobing the bill or head inside curled leavesor picking at the leavesfrom severalangles.Scoresfor
individual dead-leaf specialistsin responseto
dead leaves ranged from 3.9 to 4.8, and were
significantlyhigherthan scoresfor either of the
other two foraginggroups(K-S tests,P < 0.001).
These resultswere significantif the two deadleaflng specieswere tested separatelyagainst
ß
Dead leaf
[]
Live leaf
P < 0.02).
FEEDING EXPERIMENTS
I tested 17 individuals of five antwren species
in the outdoorcage.Theseincludedsevendeadleaf specialists(five leucophthalma
and two orDead-leaf
Generalssis
Lwe lear
nata), five live-leaf foragers(three axillarisand
speoal•s•s
(20)
•oragers
(50)
(23)
two longipennis),
and five of the generalisthauxwelli. Becauseof the small sample sizes,all inFig. 5. Median responsescoresfor three groups
with dead-and livedividualsof eachforaging modeare combined of captiveantwrenspresented
leaf substrates.Number of trials in parentheses.
in most of the following comparisons.
368
KENNETH
V. ROSENBERG
[Auk, Vol. 110
TABLE3. Prey selectivityby captiveantwrens.Median responsescores(with proportionof prey eaten in
parentheses)for eachof 12 prey categories.
a
Dead-leafspecialists
Generalists
(n = 7)
Median
Prey type
Orthoptera
Katydid/cricket
Grasshopper
Walking-stick
Roach
N
(proportion)
71
39
15
4.0 (0.93)
2.0 (0.74)
1.0 (0.40)
Live-leaf foragers
(n = 5)
(n = 5)
Median
N
(proportion)
Median
N
(proportion)
37
38
5
4.0 (0.92)
3.0 (0.74)
3.0 (0.80)
57
18
16
4.0 (0.84)
1.5 (0.56)
3.0 (0.75
4.0 (0.90
10
4.0 (1.00)
7
4.0 (0.86)
10
Spider
13
4.0 (0.92)
10
4.0 (0.90)
9
4.0 (1.00
Beetle
17
1.0 (0.18)
9
0.0 (0.22)
7
0.0 (0.00
Heteroptera
20
1.0 (0.26)
17
0.0 (0.24)
8
0.5 (0.38
9
0.0 (0.00)
2
0.5 (0.00)
6
0.0 (0.00
10
4
5
5
217
3.5 (0.80)
2.0 (0.50)
0.0 (0.00)
4.0 (1.00)
2.2 (0.56)
2
3
5
4
140
2.5 (1.00)
4.0 (1.00)
0.0 (0.00)
1.0 (0.25)
2.2 (0.58)
7
2
3
3
146
1.0 (0.43
2.5 (0.50
1.0 (0.33
Ant
Butterfly/moth
Dragonfly
Fly/wasp
Larva
Average
3.0 (0.67
2.0 (0.53
refers to number of individuals tested,while N indicatesnumber of prey items offered.
eachof the other three species.Responsescores nored. Finally, individual hauxwelliand axillaris
for live leaves, however, were not elevated in
each caught small lizards (total length ca. 50
the dead-leaf-specialistspecies.In six trials, I mm), which were beaten on a branch and swalnor ornata
presenteddead-leafspecialistswith live leaves lowed whole; neither leucophthalma
that were rolled or folded. Responsescoreswere would eat small lizards or frogs,although a leuthe sameas for dead leaves (median = 4.2), with
cophthalma
was very interestedin a lizard that
the birds picking at and probing inside the was apparentlytoo large to catch.
Becauseorthopteranswere an important food
leaves for hidden prey.
Preyselectivity.--Individualsof eachforaging for all species,I further evaluatedselectivityof
group exhibited a similar degree of selectivity, theseprey with regardto size,color,and backbasedon 12 prey categoriesofferedto eachspe- ground substrate.All speciesreadily ate most
cies(Table 3). All individuals readily ate roach- orthopterans25 mm or smaller in length (Fig.
es,spiders,cricketsand small katydids.In most 6). Reaction to larger prey, however, varied
cases,theseprey were immediatelyand eagerly among groups,with the live-leaf foragerseatcapturedand swallowed whole, sometimesbe- ing fewer large prey. Myrmotherulaaxillarisate
fore my handwasremovedfrom the cage.Larger katydidsalso were usually capturedimmediately, but were taken to a low perch to eat
(seebelow).Other orthopterans,especiallyhardbodied or brightly colored grasshoppers(Acri~
didae), were either eaten after some initial hes-
only two of six katydids greater than 30 mm
(maximum = 40 mm), and longipennisdid not
attackany of four katydidsgreaterthan 25 mm.
In contrast,the two dead-leaf-specialistspecies
collectivelyate 11 of 12 katydidsgreater than
30 mm, including four that were 48 to 50 mm;
thesepreywere morethan two-thirdsthe length
itation or were rejected.Nearly all ants, flies,
wasps,and mostbeetlesand heteropteransalso of the bird. In casesin which prey were not
were ignored or rejected.Individuals of both eaten, the birds usually showed great interest
dead-leaf-specialistand nonspecialistspeciesate in the katydids,but either were hesitantto atbutterfliesand dragonflies,often pursuingthem tackor seemedphysicallyincapableof grabbing
in the cage with uncharacteristic agility. Re- and subduingthe prey. When theselarge prey
sponseto larvaewas variable;samplesof these were capturedby one of the dead-leafspecialprey were too small to draw any general con- ists,it was usuallywith great difficulty, someclusions.
timestaking up to 12 min for the bird to catch
In addition to theseprey categories,I offered the katydid and up to 3 min to kill it (seedata
opiliones ("daddy long-legs") to ornata (1), on handling times below). The birds would
hauxwelli (2), and longipennis(2); all were ig- sometimes"give up" severaltimesbeforeeven-
April 1993]
Diet Selection
in Amazonian
Antwrens
Dead-leaf
speciallate
Live-leaf
Generallate
Dead-leaf
foragers
113)
369
specialisis
Nonspecialists
(5)
o
Prey size (mm)
Fig. 6. Proportionof orthopteranprey of different
sizeseatenby threegroupsof captiveantwrens.Number of feeding trials in parentheses.
Fig. 8. Proportion of prey eaten by specialistand
nonspecialist antwrens; prey were either cryptic
(green)on live leaves(LL), contrastingon live leaves,
hidden inside dead leaves (DL), or visible on dead
leaves.Number of feeding trials in parentheses.
tually completing the kill, a situation unlikely
to occur in the wild.
Responseto prey of different colorswas evaluated, consideringonly orthopteranslessthan
30 ram, to eliminateprey that were too large to
eat.The proportionof brown versusgreenprey
curled dead leaves.The dead-leaf-foragingspecies found 10 of 16 (71%) cryptic prey on live
leavesand 16 of 19 (84%) prey hidden in dead
leaves(Fig. 8). Nonspecialistspecieslocatedall
visible prey, but found only 16 of 23 (70%) that
eatendid not differamongdead-leafspecialists, were
live-leaf foragers,and generalists(Fig. 7); in all
cases,slightly moregreenthan brown prey were
taken. Both of these color groups were cryptic
on their respectivebackgroundsof deador live
leaves. Prey of other (noncryptic) colorswere
eaten with lower frequency, at least in the liveleating and generalistspecies.
Finally, I compareddead-leaf specialistswith
all other speciesasto their ability to locateprey
on dead-
versus live-leaf
substrates.
In these
trials, prey were either cryptic (green) on live
leaves,contrastinglycoloredon live leaves,vis-
hidden
in dead leaves. The amount
of time
taken to locateprey was highly variable among
trials and did not differ among species.My impressionwas that individual dead-leaf foragers
often did not recognizecrypticprey hiding on
live leavesand discoveredthem "accidentally"
after jostling the leavesin the cage.
Behavioralflexibility.--In three individual
hauxwelli,I tested for short-term changesin
search behavior
due to food reinforcement.
In
each case,after testing the bird's responseto
dead- and live-leaf substrates as described above,
ible on dead leaves, or hidden from view inside
(7)
ß
Dead-leafspeclahSts
[]
Live-meal
foragers
C] Generahats
Brown
Green
Other
Color
Fig. 7. Proportionof orthopteranprey of different
colorseaten by three groupsof captiveantwrens.
ß Before
•
[]After •
Indiv. 1
Indiv. 2
Indiv. 3
(is)
Total
Fig. 9. Average responsescoresof three M. hauxwellito dead-leafsubstratesbeforeand after receiving
food in dead leaves;number of trials in parentheses.
370
KENNETH
V. ROSENBERG
40
A.Dead-leaf
specialists
35
/
30
[Auk,Vol. 110
havior may be induced by food reinforcement,
at least in the generalistspecies.
Prey handlingbehaviorand times.--All species
exhibited similar modes of killing and eating
arthropodprey.The mostcommonmethod,used
for all small prey, was to crush in the bill by
working the arthropod sideways across the
mandibles,and then to swallow it whole. Larger prey, especiallylarge orthopterans,typically
were taken to a low perch within 5 cm of the
cagefloor. There the bird would begin at the
head and--by beating, shaking,and biting,-would eat the arthropodin pieces.Prey items
were frequently dropped to the floor and retrieved from the low perch. After eating (or
discarding)the head, the bird would eviscerate
(r
2
=
0.67)
25
20
5
10
15
20
25
30
35
40
45
50
and eat the thorax from the head-end first, then
5
0
10
20
15
= .!
2o
25
3o
. . .......
35
4o
45
5o
C. Live-leaf foragers
(r2 = 0.66)
5
Preysize(mm)
Fig. 10. Handling times for orthopteran prey in
three groupsof antwrens.Exponentialcurvesfit by
programCricket-Graph(Macintosh).
break off and swallow legs,then evisceratethe
abdomen, and finally after much beating and
mandibulating,swallow the exoskeletonof the
abdomen.This highly stereotypedprocesswas
alsoobservedin wild antwrenseatinglarge orthopterans.
Handling time for orthopteransup to about
20 mm was usuallynegligible,often under t0 s
(Fig. t0). For larger prey, handling time increasedsharply; usually, severalminutes were
requiredto dismemberkatydidslarger than 25
mm, and up to 40 min were spenton the largest
prey. A few orthopteransup to 26 mm were
eatenmore quickly, however, correspondingto
the upper limit of prey found in natural diets
of most species.
DISCUSSION
Resultsof this studydemonstratethat in spite
of large differencesin substrateuseand differencesin prey availability of those substrates,
antwrens prefer to eat similar kinds of prey.
food reward. In all three individuals, the reObservationsof wild and captive birds reveal
sponseto deadleaveswashigher after foodwas a fundamentaldifferencein the way thesebirds
provided than before (Fig. 9). Individual 3 searchfor prey, however. Birds that normally
showed characteristicdead-leaf searchingbe- forageon live foliage searchdirectly for prey,
haviorafter feedingat the deadleaf, repeatedly selectingfood from the array of availableprey
manipulating and probing inside leavesin all types.In contrast,dead-leafforagerssearchfor
seven subsequent trials. The other individuals
suitablesubstrates
and then closelyinspectthese
each manipulated at least one dead leaf after for hidden prey, taking prey roughly in profeeding, whereasneither had even touched a portion to what is availablein the leaves.Deadleaf with the bill before.Responseto live leaves leaf specialistsdid not, however, exhibit a greatwas not elevated in any bird. Although this er overall selectivityof prey, nor a greatertensmall samplewas not appropriatefor statistical dencyto avoid prey not normally encountered
testing,it suggeststhat dead-leafsearchingbe- in nature. I conclude,therefore, that this speI provided food only in the dead leaf. After 10
consecutivefeedings,I retestedtheseindividuals' responseto substratesin the absenceof a
April 1993]
DietSelection
in Amazonian
Antwrens
cialization is achieved through a change in
searchbehavior and is not accompaniedby an
equivalentchangein prey preference.
Robinsonand Holmes (1982) recognizedthe
"substrate-restricted"searching mode, represented by the behavior of the Black-capped
Chickadee(Parusatricapillus),
asone of five foraging modesseen in insectivorousbirds in a
northern hardwoods forest. Chickadees, like the
antwrens, searchedspecificsubstratesfor hidden prey, but were opportunisticasto typesof
substratessearched. Greenberg (1987a) demonstrated
that hand-raised
Carolina
Chickadees
(P. carolinensis)
exhibitedexploratorybehavior,
but showed no consistentpreference for particular substratetypes.In contrast,hand-raised
Worm-eatingWarblers(Helmitheros
vermivorus),
a dead-leaf specialistin winter, showed an innatetendencyto exploredeadleavesmorethan
other substrates.Greenberg (1987a) contrasted
the presenceof exploratoryand manipulative
behavior in speciesthat normally searchfor
hiddenprey ("insurface"foraging)with the lack
of such behavior in birds that forage on leaf
surfaces.
The
antwrens
I studied
exhibited
a
similar contrast in degree of exploratory behavior associatedwith degree of insurfaceversus surfaceforaging. These behaviors may remain somewhat
flexible
to allow
for short-term
learning of local food abundances,assuggested
by the temporaryincreasein dead-leafsearching behavior seenin the mostgeneralized species,hauxwelli.
Greenbergfurther demonstrated
that behavioral plasticity in adult birds is relatedto degreeof neophiliashownby juveniles
in responseto novel stimuli. Exploratory behaviors usedin dead-leafforaging might representa neotenicretention of neophilia, which
is usuallyextinguishedby sixto eight weeksof
age (Greenberg 1987a).
Substrate-restricted
foraging was associated
with reduced diet breadth and greater stereotypy amongindividuals (low PDH), compared
with the substrategeneralist hauxwelli.However, dead- and live-leaf-foraging specieswere
equallystereotyped,suggestingthat both groups
perceivedtheir prey baseaspredictable.In this
sense,both dead- and live-leaf-foraging birds
may be consideredevolutionarily specialized
(Sherry 1990).The mostconsistentdietary difference between dead-leaf-specialistand other
antwren specieswas the larger average prey
size, and especiallylarger orthopterans,taken
371
by the dead-leaf foragers.Becausespecialization on dead leavesimposesa costin terms of
lower foraging rates,and probably lower capture rates, compared with live-leaf foragers
(Thiollay 1988,Rosenberg1990a),the ability to
take larger prey may be particularlyimportant
in these birds.
The maintenanceof innate and highly stereotypedbehaviorsthat restrictsearchingto one
particularsubstratemustultimately dependon
the productivity of that substrate.Suspended
dead leaves have been shown
to be abundant
in many tropical forest habitats, to support
higher densitiesof arthropodsthan live foliage,
and to be among the least seasonalof tropical
forest resources(Greenberg1987b,Boinskiand
Fowler 1989,Rosenberg1990a,b). Comparisons
of antwren diets and prey availability in my
study further demonstrated that dead leaves
provide a higher proportionof preferred prey
types. The relative abundanceof larger prey,
especiallylargeorthopterans,maybe the single
mostimportant factorpromoting specialization
on dead leaves.Dead-leaf specialists,therefore,
can searchonly these substrateswith a high
probabilityof finding acceptablepreyand a low
chanceof encounteringunsuitableprey (mainly ants).More generalizedlive-foliagesearchers
encountera wider array of potential prey types
and find a smaller proportion of these prey acceptable.That both specialistsand generalists
will eat a greater variety of prey in captivity
than in the wild, however, suggeststhat natural
diets are constrainedby both availability and
the ability of the birds to catchand handle certain prey. For example,antwrensprobablyrarely can catch butterflies, dragonflies,or lizards
in the wild, but will eat them if given the opportunity. Thus, even substrate specialists
maintaina degreeof plasticityin termsof prey
selection.
All speciesof antwrensstudiedpreferentially
selectedorthopterans.Heavy predation on Orthopteraby tropicalinsectivoreshaspreviously
been recognizedasone of the fundamentaldifferencesbetween these speciesand insectivorous birds of the Temperate Zone, which eat
primarily caterpillarsduring the breeding season (Greenberg 1981,Thiollay 1988). The diets
of other dead-leaf specialists(mostly Furnariidae) contained large proportions of orthopterans (Rosenberg1990a),as did the diets of four
species of woodcreepers (Dendrocolaptidae;
372
KENNETH
V. ROSENBERG
Chapmanand Rosenberg1991),whereasother
[Auk,Vol. 110
serv.). During feeding trials, antwrens some-
timesengagedin prolonged"tug-of-wars"with
tropicalflycatchers
(Sherry1984).Orthopterans large katydidsbefore successfullydislodging
prey were more important to a guild of Neo-
were barely represented in the diets of temperate forest birds (e.g. Robinson and Holmes
1982), but grasshoppers(Acrididae) were important,at leastseasonally,to speciesin shrubsteppeand desert riparian habitats (Rotenberry
1980, Rosenberg et al. 1982). Most identified
orthopteranseatenby tropicalspecieswere ka-
tydidsand crickets(suborderEnsifera),rather
than Acrididae. Katydids and cricketstend to
be soft-bodied,crypticallycolored,and usually
active nocturnally, while hiding motionless
during the day (Belwood1990).Acrididsappear
to be mostly diurnal, perching conspicuously
and avoiding capture by jumping (pers. observ.). During feeding trials, both dead- and
them from the substrates.I suspect,therefore,
that the added depth (strength)of the bill, and
especiallythe hookedtip, rather than the added
length, enablesthese tropical birds to handle
such large prey. Antwrens, and apparently all
antbirds,rely entirely on the bill when manipulating and dismembering large prey. Some
other birds, suchasfoliage-gleaners(Automolus,
Philydor), greenlets (Hylophilus),and barbets
(Capito,
Eubucco),
usethe footto hold preyagainst
a branch while eating the prey (pers. observ.).
This behavioral innovation greatly facilitates
prey handlingand reduceshandlingtimes.That
captive antwrens would eat larger prey than
thosefound in natural diets suggeststhat prey
sizemaybe limited moreby handling time than
live-leaf-foraging antwrens reacted differently
to these two kinds of orthopterans. Whereas by the physicalcapabilitiesof the birds.While
nearly all ensiferanswere quickly and eagerly manipulatingand eating prey, thesebirds may
be more vulnerable (i.e. more conspicuousand
bodied and brightly colored, tended to be ig- lessvigilant) than during other foragingactivnored or eaten only after initial rejection. Sev- ities. Furthermore,long periods of prey haneral acridids, including a common speciesof dling causesbirds to lag behind the mixed-spespur-throated grasshopper (Cyrtacanthacridi- ciesflocksin which they forage.
nae), obviously were distasteful to the birds;
Although antwren specieseat similar kinds
after initial attacks the birds would often bill
of prey at grosstaxonomiclevels, it is likely
wipe vigorously or show visible discomfort. that they overlap little in the speciesof arthroMany of these insectswere eventually eaten, podsthat they encounterand eat. For example,
however, without apparent ill effects. Ant- katydids show species-specific
preferencesfor
consumed, acridids, which were often hard-
wrens also appeared to recognize or react to
diurnal roosting sites;individuals in dead and
other prey asbeing distasteful.Theseincluded live leavesrepresent different species(Belwood
most stink-bugs (Pentatomidae),some caterpil- 1990).The lack of greater taxonomicresolution
lars and butterflies, and all opiliones. These in this and other dietary analysesmay limit
behaviors did not differ, however, between
inferencesthat can be made about resourcepardead-leaf-specialist
speciesand other speciesof titioning and potential competition. If, howantwrens.
ever, diet categoriesreflect both taxonomicand
Greenberg (1981) noted that tropical insec- ecological similarities among prey (e.g. comtivores have longer and narrower bills than bining all larvae,separatingroachesfrom other
equivalent-sizedtemperatespecies,and attrib- orthopterans),then further subdivisionmay add
uted this differenceto the efficiencyof captur- little information about predator-preyrelationing the largestprey types in each region (or- ships(Cooperet al. 1990).Becauseantwrens do
thopterans versus caterpillars). Besidesbeing not appear to discriminate among subtle varilonger, antwren bills are considerablydeeper ationsin their preferredprey types(e.g.brown
(i.e. heavier) than those of small North Amer- versusgreen katydids),it is unlikely that speican insectivores(e.g. Parulinae) and are dis- cificcoadaptationsexistbetweenparticularbird
tinctly hookedat the tip. Although Greenberg and arthropod species.Furthermore, specialists
(1981) reasonedthat longer bills are adaptive were not more discriminatorythan generalists,
for capturing"highly mobile"orthopterans,
the suggestingthat limiting encounter to only a
primaryantipredatorbehaviorof largekatydids few prey species(thoseinhabiting deadleaves)
is to remain motionlessand tightly grip the doesnot necessarilyinfluencecriteria for prey
substrate (Belwood 1990, Rosenberg pers. ob- choice.
April 1993]
DietSelection
in Amazonian
Antwrens
Foraging experiments with caged birds have
proven useful in studiesof learning ability (e.g.
Heinrich and Collins 1983, Greenberg 1984,
1987a),microhabitatpatch use (Zach and Falls
1976),vigilance(e.g.Waite 1987),and prey-handling ability (e.g. Daviesand Green 1976,Chai
1986),as well as prey discriminationand preference(e.g.Sherryand McDade 1982,Chai 1986,
Greig-Smith 1987). These studies used both
hand-reared and wild-caught birds, usually in
a temporaryaviary setting.Although it wasnot
possibleto maintain a captivepopulationof antwrens in my study, these birds were excellent
subjectsfor short-term experiments. Working
with captive birds allowed me to distinguish
betweenprey choiceand responseto prey availability, and provided the opportunity to observeand measurespecificaspectsof prey capture and handling not possiblewith only wild
birds. The successof this approachmay have
been fortuitous,however, and may vary with
the type of bird studied.For example,I attempted the sameprotocolwith two individuals each
of two other antbird species(Hypocnemis
cantator and Thamnomanes
schistogynus);
none of
these birds showed signsof adjusting to captivity, and none acceptedany food in their cages.
Whenever possible,however, experimentswith
wild birds, in combination with field data on
prey availability and use,will enhancestudies
of foraging behavior and diet selection.
I
ACKNOWLEDGMENTS
I thank J. V. Remsen, Jr., T. A. Parker III, and J.P.
(LSUMNS)providedan unparalleledatmospherein
to conduct this research. I benefitted
from dis-
cussionswith J. Belwood,R. J. Cooper, T. L. Erwin,
R. Greenberg,C. Munn, T. W. Sherry,and D. F. Stotz,
among others.Field work in Pando,Bolivia, was made
possiblethrough expedition funds of the LSUMNS
and a grant by the National GeographicSocietyto J.
V. Remsen,Jr. Membersof this and other expeditions
helped collectspecimensfor dietary analysis.G. Servat of the Museo de FIistoria Natural Javier Prada,
Lima, Peru, provided additional stomachcontentsof
Peruvian antwrens. For the opportunity to work at
the TambopataReservein Peru, I thank Max Gunther
D. for accessto the Explorer'sInn. Chris Canadayand
Robb
Brumfield
were
invaluable
field
assistants
insect identifications. The LSU Entomology Museum
loaned collecting equipment and also helped with
identifications;A. Rypstra and K. Canigliaro also
kindly loaned equipment for collecting insectsand
building cagesat Tambopata.Various drafts of this
manuscriptbenefitted from commentsby A. Afton,
J. M. Bates,K. M. Brown, S. J. Hackett, R. B. Hamilton,
P. P. Marra, T. A. Parker III, D. P. Pashley,J. V. Remsen,Jr.,J. T. Rotenberry,T. S. Sillett, R. M. Zink, and
two anonymous reviewers. My research was supported by a National ScienceFoundation dissertation
improvement grant (BSR-8800905),an LSU Alumni
Federation Fellowship, a Charles M. Fugler fellowship in tropical biology, and research funds from
LSUMNS and LSU Departmentof Zoologyand Physiology.
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