Leadership of Winter Mixed-Species Flocks by Tufted Titmice (Baeolophus bicolor): Are Titmice Passive Nuclear Species?

Abstract

The tufted titmouse (Baeolophus bicolor, TUTI) is a nuclear species in winter foraging flocks whose antipredator calls are used to manage predation risk by diverse heterospecifics. We hypothesized that satellite species in mixed flocks follow TUTI (not vice versa), thereby defining the role of TUTI as a "passive" nuclear species. We followed 20 winter mixed-species flocks in North-Cen-tral Florida and assessed angular-angular correlations between overall flock, TUTI, and satellite species movement directions. We observed significant correlations between overall flock movement directions and those of TUTI, confirming our central prediction. Within flocks, however, fine-scale movement directions of satellite species were often more highly correlated with those of other satellites than with TUTI movements. We conclude that TUTI are passive nuclear species whose movements define flock paths, but within flocks, TUTI movements may have less influence on satellite movements than do other factors.

Full text

Hindawi Publishing Corporation
International Journal of Zoology
Volume 2011, Article ID 670548, 11 pages
doi:10.1155/2011/670548
Research Article
Leadership of Winter Mixed-Species Flocks by Tufted Titmice
(
Baeolophus bicolor
): Are Titmice Passive Nuclear Species?
Thomas A. Contreras1and Kathryn E. Sieving2
1Biology Department, Washington and Jefferson College, 60 S. Lincoln Street, Washington, PA 15301, USA
2Department of Wildlife Ecology and Conservation, University of Florida, Gainesville, FL 32611-0430, USA
Correspondence should be addressed to Thomas A. Contreras, tcontreras@washjeff.edu
Received 30 December 2010; Revised 25 March 2011; Accepted 31 May 2011
Academic Editor: Alan Afton
Copyright © 2011 T. A. Contreras and K. E. Sieving. This is an open access article distributed under the Creative Commons
Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is
properly cited.
The tufted titmouse (Baeolophus bicolor, TUTI) is a nuclear species in winter foraging flocks whose antipredator calls are used to
manage predation risk by diverse heterospecifics. We hypothesized that satellite species in mixed flocks follow TUTI (not vice
versa), thereby defining the role of TUTI as a “passive” nuclear species. We followed 20 winter mixed-species flocks in North-Cen-
tral Florida and assessed angular-angular correlations between overall flock, TUTI, and satellite species movement directions. We
observed significant correlations between overall flock movement directions and those of TUTI, confirming our central prediction.
Within flocks, however, fine-scale movement directions of satellite species were often more highly correlated with those of other
satellites than with TUTI movements. We conclude that TUTI are passive nuclear species whose movements define flock paths, but
within flocks, TUTI movements may have less influence on satellite movements than do other factors.
1. Introduction
Multispecies bird flocks, comprising individuals that move
together in organized association with each other as they for-
age during daylight hours, are a common phenomenon in
forested ecosystems of the world [1]. Flock participants
occupy different behavioral niches, or social roles, within
flocks. Flocking species are generally classified into “nuclear”
and “satellite” roles [2–4]. Nuclear species are those flock
participants whose conspicuous behaviors (distinctive alarm
or other vocalizations and active movements) enhance flock
cohesion and may stimulate flock formation. Nuclear species
are typically intraspecifically social (occurring in extended
family groups for some of the year), and they occur more
often in flocks than outside of them when flocks occur [5,6].
Nuclear species are thought to fall into two general catego-
ries : passive or active nuclear species [2,3]. Passive nuclearity
is hypothesized to come about when satellite species actively
seek out and follow the nuclear species, thereby defining the
nuclear species as the flock leader. Conversely, active nuclear
species are hypothesized to seek out and join existing mixed-
species flocks and are just as likely to follow the satellites as
to be followed by satellites, but active nuclear species are still
able to maintain flock cohesion (see review in Farley et al.
[4]). A variety of fitness benefits can accrue to satellite species
as a result of flocking with nuclear species, but benefits to
nuclear species are less obvious [7–12].
Parids (family Paridae) function as nuclear species in
winter and nonbreeding mixed-species forest flocks in North
America and elsewhere in the Holarctic [4,7–9,13]. As a
family, parids have traits that predispose them to nuclear
roles in heterospecific groups; they are intraspecifically social
[1,14,15] and aggressive mobbers of potential predators,
usually leading mobbing events; their behavior may signifi-
cantly reduce predation risk for satellite species [4,11,13,14,
16–19]. In the Eastern United States of America, the tufted
titmouse (TUTI; Baeolophus bicolor) is a socially dominant
parid that functions as a nuclear species in flocks even where
TUTI co-occur with chickadees in flocks (chickadees may
also serve as nuclear species when not participating in flocks
with TUTI [14]). TUTI, like other parids, produce copious
threat-related vocalizations that are thought to be signals
meant for conspecifics but that are used as informational
cues by numerous heterospecifics [19–22]. Some parids give

2International Journal of Zoology
food-related cues for conspecifics [23], but their use by het-
erospecifics has not been documented to our knowledge.
Thus, the central known fitness benefits available to satel-
lite species, or heterospecific associates of parids more gener-
ally, may be the reduction of predation risk during critical
activities [9,19]. Dolby and Grubb Jr. [7] demonstrated that
when TUTI were removed from isolated woodlots, individu-
als of satellite species remaining in those woodlots in winter
occupied reduced foraging niches, avoided exposed foraging
sites, and declined in overall physical condition relative to
individuals who were in woodlots where TUTI had not
been removed. The presence of parids enhances access to
resources and microhabitats within forest bird home ranges
([9]; aids heterospecifics in finding suitable breeding habitat
via heterospecific attraction; [24]) and possibly increases
nest success [25]. These findings suggest that the prodigious
amount of information that parids produce concerning their
immediate perceptions of predation risk aids their fellow
prey species in many aspects of decision making including
(a) increased foraging efficiency, (b) access to critical micro-
and macrohabitats, and (c) an elevation of the effectiveness
of antipredator defense [10,19,22,25,26].
Determination of whether nuclear species interact with
heterospecifics passively or actively in mixed flocks has only
received speculation at this point [10], yet this kind of infor-
mation could enhance understanding of the evolutionary
ecology of facilitation, parasitism, and mutualism in animal
communities [27]. For example, if titmice are active nuclear
species, soliciting close relationships with other species, it
would suggest that they accrue benefits from associated
heterospecifics [28].Inthiscase,itmightbeproductiveto
test whether the finely tuned antipredator calls of tufted
titmice may involve active signaling to heterospecifics rather
than being purely intraspecific (kin) signals that are gleaned
by eavesdropping heterospecifics [15].If,however,titmice
are passive flock leaders being followed by other species, then
exploring aspects of heterospecific exploitation of the nuclear
species would be most productive [10]. To date, we have
conflicting evidence regarding what tufted titmice may gain
in the presence of heterospecifics. One potential benefit is
food items taken from smaller satellites (kleptoparasitism;
[29]). However, we have witnessed that the only species in
actively foraging mixed flocks that reliably get killed during
hawk attacks are titmice (T. A. Contreras and K. E. Sieving,
unpublished data), suggesting that the presence of flocks may
be an important fitness cost to titmice. Here, we sought
to determine whether TUTI are passive or active nuclear
species in order to inform future research questions and
critically assess the common assumption that mixed-species
bird flocks are models of mutualism [30]. If satellite and
nuclear species are not gaining fitness through association,
then it would be more productive to assume that the
full range of exploitative (parasitic and commensal) and
mutualistic relationships are displayed in flocks [10,27,31].
We undertook an analysis to distinguish active from passive
flock leadership by TUTI in order to clarify future steps in
understanding the ecological and evolutionary relationships
acting within mixed species flocks.
Studies in North-Central Florida [4,9,16,17] and else-
where in Eastern NA (see Greenberg [1]) identify TUTI as
the primary nuclear species in most winter mixed-species
bird flocks. While this classification of TUTI is based on
their pervasive presence in winter foraging flocks and their
dominating role in mixed-species mobbing flocks [7,9], the
question remains whether TUTI are functioning as passive
or active nuclear species in winter foraging flocks. Accord-
ingly, we used a correlative analysis of TUTI and satellite
movements at two spatial scales of flocking behavior which
we categorized as: (1) the correlation between the movement
of TUTI or satellites with overall flock movement through
a landscape (flock leadership) and (2) the correlation between
the movement of TUTI or satellites with the movement of
immediate flock members (within-flock movement).
We followed mixed-species flocks during a single winter
(2004) in North-Central Florida, mapping the overall move-
ment directions of flocks and the movement directions of
randomly selected satellite species and TUTI in each flock
(providing comparisons for both analyses; flock leadership,
and within-flock movements). Based on Farley et al. [4], we
classified individuals in the flock as nuclear species (TUTI),
satellite species (species who are “regular and occasional
associates” in mixed-species flocks), or nonflocking species.
If TUTI are functioning as passive nuclear species and flock
leaders, then we predicted that (1) overall flock movement
direction should be more highly correlated with the move-
ment direction of individual TUTI than with those of satellite
species (Figure 1(a)) and (2) the within-flock movement
directions of satellite species in flocks should be more highly
correlated with the movement direction of the nearest TUTI
than with the nearest satellite species (Figure 1(b)).
Previous observations of forest bird mobbing activity
(see Sieving et al. [9]) also suggest that satellite species may be
more likely to move through areas with less vegetative cover
(open cover types) when TUTI are present, especially when
perceived or actual risk of predation may be high. There-
fore, we also predicted stronger correlations between TUTI
movement direction and flock movement direction as flocks
move through more open cover types.
2. Materials and Methods
2.1. Study System. To test our predictions, we observed and
followed wintering mixed-species: forest passerine flocks in
North-Central Florida from January to March, 2004. Flocks
were observed at 3 sites: (1) the University of Florida’s
Ordway-Swisher Biological Station (Putnam County; N
29◦4145.6,W81
◦5856.2), (2) the San Felasco Ham-
mock Preserve State Park (Alachua County; N 29◦4246.3 ,
W82
◦2723.7), and (3) Payne’s Prairie Preserve State Park
(Bolen’s Blufflocation; Alachua County; N 29◦3324.6,
W82
◦1947.5). All 3 sites had similar vegetation and
cover types. In hardwood stands (cover type: hardwood),
the canopy and subcanopy layers were dominated primarily
by laurel oak (Quercus laurifolia), live oak (Q. virginiana),
sand live oak (Q. geminata), water oak (Q. nigra), pignut
hickory (Carla glabra), sweetgum (Liquidambar styraciflua),
or cabbage palm (Sabal palmetto), while the understory was

International Journal of Zoology 3
Satellite species
TUTI
(a) Hypothesized movement paths
Responding
bird Focal
bird
N
Species 2
Species 1
T1
T2
T3
T0
S1
S2
S3
(b) Diagram of flock movement
Figure 1: (a) Illustration of one example of the hypothesized relationships between the overall flock movement path (using successive flock
centers to chart the path; black line) and the movement paths of two individual flock participants: TUTI (nuclear species; dashed line) and a
satellite species (dotted line). (b) Diagram of a 15-minute portion of a flock movement path with T0,T1,T2,andT3representing estimated
flock centers at 0, 5, 10, and 15 minutes respectively. Lines S1,S2,andS3represent “movement” segments between estimated flock centers,
with the length of the line representing the movement distance of the flock and the arrow showing the overall flock movement direction
(azimuth) between flock centers. Dashed lines (SPECIES 1 and SPECIES 2) represent the observed movements of 2 randomly selected birds
observed while at flock center T1 (to be correlated with flock path). Dashed lines at T3 represent the movements of a FOCAL BIRD and a
RESPONDING BIRD (an individual in the same general area that moves immediately after the focal individual moves) to be correlated with
each other for within-flock analysis. These observations were made at all flock centers.
dominated by Ilex spp., Lyonia spp., and saw palmetto
(Serenoa repens). More open habitats (cover type: open) used
in the study generally had a sparse overstory of widely dis-
persed mature longleaf pine (Pinus palustris) with a patchily
distributed subcanopy of Quercus spp. (primarily turkey oak
(Quercus laevis) and sand live oak), and rosemary (Ceratiola
ericoides), and understory dominated by wiregrass (Aristrida
stricta), exotic grasses, saw palmetto, and various forms.
Flocks occurred throughout the woodland communities of
our study areas, and we sought replicate samples in 3
major cover types that were identified as (a) hardwood and
(b) pine-dominated (open) forest and (c) the boundaries
between these two major forest classifications. Indeed, flock
dynamics varied across these three habit designations, and
we included them as predictors in our analyses (see below).
2.2. Flock Observations and Data Collection. Mixed-species
flocks without TUTI are rarely observed in our study region
[4]; therefore, we systematically searched each of the 3 study
areas for the presence of TUTI using existing trails and roads,
and then initiated observations of the associated flocks.
To reduce the possibility of pseudoreplication of individual
and flock movement data, we never surveyed any specific
area more than once and each flock observed was at least
350 m from any other flocks observed, based on maximum
reported TUTI winter home range sizes [17,32]. Once lo-
cated, flocks were followed for a minimum of 15 minutes,
allowing birds to become acclimated to the observer (T. A.
Contreras in all cases). Flocks were considered acclimated
when birds stopped approaching the observer, and alarm
calls were infrequent or directed at other bird species. After
acclimation, we followed the flock for a maximum of 55
minutes.
2.2.1. Flock Leadership Data. We collected data for determin-
ing flock leadership at 5-minute intervals, and during each
interval, we (1) estimated and marked the center of the flock
(based on the area of the aggregation with the greatest esti-
mated number of birds) by placing a wire flag in the ground,
(2) identified the flocking species and estimated the number
of individuals present in the flock, and (3) estimated the
movement azimuth (degrees), of multiple randomly selected
TUTI and satellite focal individuals at each flock center
(azimuths of sampled individuals were estimated from the
flock center using a compass; Figure 1(b)). If we lost track of
a flock during the observation period, we then searched for
anewflocktoobserve.
2.2.2. Within-Flock Movement Data. During each 5-minute
interval, we estimated the direction and distance of move-
ments made by randomly selected individuals in the flock
and of the next movement made by another flock participant
that was closest to the first bird, assuming that the “respond-
ing individual” was moving in response to the movement of
the focal individual. These estimates were used for determin-
ing within-flock movement correlations (Figure 1(b)). To
maximize the potential that the responding bird was actually
responding to, or aware of, the focal bird’s movement, the
second bird had to be within 5 m of the focal bird’s initial
position and had to move within 60 seconds of the focal
bird’s movement; otherwise, we selected a new focal bird and
responding individual. And if, within a flock, we lost track of
individuals under observation, we selected a new focal bird
and responding individual.
To randomly select individuals for observations (both
“flock leadership” and “within flock movement”), at each
flock center, we started at a randomly selected azimuth and

4International Journal of Zoology
then scanned the flock in a clockwise direction for the first
focal individual that moved more than 5 m horizontally. We
then estimated the movement distance (using a range-finder)
and the movement direction (azimuth) of that individual.
The azimuth for each individual was estimated from the
initial point where the individual was observed. In some
cases, this often meant marking the initial and subsequent
horizontal positions with pin flags and then returning later
to obtain measurements. Although individuals within flocks
were not marked and could have been observed more than
once within each flock, randomizing the selection of flock
members for observations, and the relatively large number
of individuals per flock may has reduced the probability
of pseudoreplication of observations of individual flock
participants.
2.2.3. Characterization of Flock Path and Habitat. After ob-
servations were completed for each flock, we determined the
overall path of each flock. We returned to the first flock center
observed (which had been flagged) and measured its position
using a global positioning system (GPS, accuracy ±3m;
Garmin GPSMap 76, Garmin International Inc., Olathe,
Kan, USA). The distance and direction (azimuth) of each
subsequent flock center relative to the previous flock center
was measured using a compass and range finder and then
plotted by connecting lines between successive flock centers
(Figure 1(b)). Distances between flock centers ranged from
0–131 m with a mean distance of 32 ±21 m (±SD).
At each of the flock centers, we recorded the “cover type”
that the flock and individuals moved through (for each
5-min segment of movement): (1) hardwood, (2) open (gen-
erally pine sandhill or other pine stands with sparse canopy
cover), and (3) boundary, for example, the flock crossed
the boundary between hardwood and pine cover types
during a 5-minute segment. Using the GPS to find the
approximate position of the first flock center allowed us to
plot the overall path using a GIS (ArcView v3.2, ESRI,
Redlands, Calif, USA) to view flock centers overlaid on digital
orthophoto quarter-quadrangles with 1-m resolution (1999;
Land Boundary Information System (LABINS), Florida
Dept. of Environmental Protection, Bureau of Survey and
Mapping, Tallahassee, Fla, USA) and confirm cover types for
each subsequent flock center. In addition, within a 0.05-ha
circle surrounding each estimated flock center, we estimated
(1)theproportionsofoverheadcanopy(e.g.,emergent,
dominant, and codominant crown classes) and subcanopy
cover using a densitometer, (2) the density of large stems
>5-cm diameter at breast height (DBH) using the point-
quarter method [33], and (3) the number of small stems
<5-cm DBH but >1 m in height within the 0.05-ha circle.
We predicted that there would be significant differences
between hardwood and open cover types in one or more
of the vegetation characteristics, and this might help inform
our interpretations of movement patterns; that is, birds may
move faster or slower through more open habitats, and this
can influence flock cohesion [34].
2.3. Data Analysis. Two spatial scales of movements were
analyzed to assess the prediction that satellite species primar-
ily follow TUTI and not each other. First, we asked which
species are leading/directing the path of the flock (flock lead-
ership) by testing whether TUTI movement paths (direction
of movements during 5 min intervals) are more highly cor-
related with the overall flock paths than with satellite species
movement directions). Second, we tested whether individual
satellite species were tracking the fine-scale movements of
nearby titmice more so than those of nearby satellite species
(within-flock movements). For all analyses we used α=0.05
to determine statistical significance.
2.3.1. Flock Leadership. Using movement data for both flocks
and individuals for each 5-minute time segment, we first cal-
culated correlation coefficients between the azimuth for flock
movement during each of the 5-minute time intervals and
the azimuth for randomly selected individuals in the flock
during the 5-min interval. We divided analyses between
the three cover type classes where flocks were observed
(hardwood, open (pine), or boundary), and for this analysis
included further subdivisions of the data into two flock
movement distance categories (fast, >30 m/5 minutes; slow,
<30 m/5 minutes). This latter categorization was adopted,
because flock movement rates varied greatly around the
mean of 30 m/5 min; some flocks were sometimes stalled,
whereas at other times a flock could move up to 131m/5 min
(see Section 2.2.Flock Observations and Data Collection),
and we noted that movement dynamics appeared to differ
between relatively slow and fast-moving flocks. Finally,
analyses were further subdivided by flock role (nuclear
(TUTI) vs. satellite species; Table 1).
2.3.2. Within-Flock Movements. To test the prediction that
the within-flock movement direction and distance of indi-
vidual flock members would be more highly correlated with
those of the nuclear species (TUTI), we calculated correlation
coefficients (raa) and associated 95% confidence intervals
between the movement azimuths of randomly selected indi-
viduals within the flock (focal species) and the first individ-
ual to move after the focal individual moved (responding
species). As above, the data were subdivided by focal species
type (i.e., nuclear (TUTI) versus satellite species; nonflocking
species were not included in this analysis) and cover type. We
further subdivided the analyses by the movement distance of
focal species using two distance classes: individuals moved
<15 m or >15 m. These distance classes for within-flock
movement are based on the mean within-flock movement of
focal species (15.5±21 m (±SD)), and were delineated to rep-
resent biologically reasonable distinctions between exploita-
tion of a single foraging patch (within 15 m) versus changing
foraging patches (moving more than 15 m in a single move-
ment). Only movements >5 m were recorded/analyzed, since
movements of less than 5 m were very frequent and probably
correlated with movements of escaping prey rather than flock
mates.
If only conspecifics are responding to focal individu-
als, then correlations of within-flock movement directions
between focal and responding individuals would suggest that
the movement of individuals within flocks was influenced
primarily by intraspecific interactions. Therefore, we used

International Journal of Zoology 5
Tab l e 1: All species encountered in mixed-species flocks during the
study (classified into flock roles (nuclear, satellite, or nonflocking)
based on Farley et al. [4]). Percentage of flocks is the percentage of
the 20 flocks where the species was encountered at a minimum of
one observation point. Max. number of individuals is the estimated
maximum number of individuals in a flock observed at one time.
Common name Scientific name %offlocks/max.
# of individuals
Nuclear
Tufte d t i t m ouse Baeolophus bicolor 100/6
Satellite
Black-and-white warbler Mniotilta varia 50/2
Blue-gray gnatcatcher Polioptila caerulea 70/6
Blue-headed vireo Vireo solitarius 30/2
Carolina chickadee Poecile carolinensis 20/3
Downy woodpecker Picoides pubescens 40/3
(Yellow) palm warbler Dendroica
palmarum 15/15
Pine warbler Dendroica pinus 35/2
Red-bellied woodpecker Melanerpes
carolinus 30/3
Ruby-crowned kinglet Regulus calendula 95/15
White-eyed vireo Vireo griseus 15/1
Ye l l o w -t h r o a t e d w a r b l e r Dendroica
dominica 10/1
Nonflocking
Blue jay Cyanocitta cristata 5/3
Eastern bluebird Sialia sialis 5/2
Yellow-rumped warbler Dendroica coronata 15/50+
Northern parula Parula americana 10/2
White-throated sparrow Zonotrchia
albicollis 5/20
aG-test of independence to determine if there was a lack
of independence between the movement of the focal species
observed and whether or not the responding individual was
a conspecific or heterospecific. For the G-test we used a 3 ×2
contingency table with the columns being the flock role of the
focal species (nuclear vs. satellite vs. nonflocking species) and
the rows being whether or not the responding species was a
conspecific or heterospecific. Cells within the table contained
the frequency of responding individuals.
Since correlation coefficients for circular data (e.g.,
azimuths) should not be calculated using statistical tests
for linear measurements [35], we used Igor Pro statistical
software (v.6.2.1, Wavemetrics, Inc., Lake Oswego, Ore, USA)
to calculate Angular-Angular correlation coefficients (raa),
which are analogous to a Pearson’s r(see methods described
in Zar [35] and Fisher [36]) and the 95% confidence intervals
associated with each raa. If “0” did not fall within the con-
fidence interval calculated for an raa, then the correlation
coefficient was statistically significant at P<0.05 [35]. Given
the lack of significance testing options for angular correla-
tions (we found none), we relied on the 95% confidence
intervals (CI) for each raa to make inferences about whether
or not raa’s from comparable categories were biologically
different. If CI’s for correlation coefficients (in general), and
for other directional measures similar to raa’s, do not overlap,
and if the CI’s are similar in magnitude, then meaningful
differences can safely be assumed (see Nakagawa and Cuthill
[37] for discussion).
3. Results
3.1. Flock Observations. In total, 20 flocks were observed at
our study sites (13 flocks at the Ordway-Swisher Preserve, 5
flocks at the San Felasco Hammock Preserve State Park, and
2 flocks at the Payne’s Prairie Preserve State Park) with an
average of 8 flock centers mapped per flock path recorded
(range =4–12 flock centers). There was a significant dif-
ference in flock movement rates (per segment) in different
cover types (F2,131 =7.56, P=0.0007, r2=0.10). Flock
movement rates were significantly greater as flocks crossed
boundaries (12.5±4.0m/minute(±SD)) when compared to
movement rates of flocks in hardwood (6.1±4.5m/minute
(±SD)) or open (6.1±3.5m/minute (±SD)) cover types.
A total of 16 species were detected, and besides TUTI, only
two others were present in the majority of flocks observed:
Ruby-crowned Kinglets and Blue-gray Gnatcatchers which
were present in 95% and 70% of the flocks, respectively
(Table 1). Mean species richness for the 20 flocks was 5.6±
1.7 species per flock (±SD) with a mean maximum number
of individuals in each flock of 23.8 ±23.2 individuals (±SD).
Five common species observed in or near flock centers,
that are not flock participants (nonflocking species, Farley
et al. [4]; Table 1), were excluded from all analyses except
for the G-test above. Along flock paths, the proportion of
overhead canopy cover was greater in hardwood than in
open (pine) cover types (Figure 2(a)), whereas proportions
of overhead subcanopy, small stem density, and large stem
density were similar between hardwood and open cover types
(using 95% confidence intervals; Figures 2(a) and 2(b)). This
suggests that while canopy cover was different between the
two general habitat types, subcanopy and shrub cover is
similar.
3.2. Flock Leadership. We observed a total of 346 individuals
(113 TUTI and 233 satellites) whose movement directions
were correlated with flock movement at 117 flock centers. For
all cover types (slow and fast-moving flocks pooled) and for
both slow and fast-moving flocks (cover types pooled), flock
movement direction was more highly correlated with the
movement direction of TUTI than with the movement direc-
tion of satellites (Figures 3(a),3(b),and3(c)). When flocks
were moving slowly across boundaries, satellite movement
direction and flock movement direction were more highly
correlated, whereas in open (pine) cover there was a negative
correlation between flock and TUTI movement directions
(Figure 3(b)). We note relatively small sample sizes for the
latter two findings (Figure 3(b)). For fast-moving flocks
(>30 m/5 minutes; Figure 3(c)), the movement direction of
TUTI was more highly correlated with flock movement di-
rection than with the movement direction of satellite species
in all cover types. The greatest difference between correlation
coefficients calculated for TUTI and satellite species with

6International Journal of Zoology
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.9
Canopy Subcanopy
Vegetation layer
Proportion overhead cover
Hardwood
Open
1
(a) Proportion overhead cover
0
20
40
60
80
100
120
140
160
180
200
Hardwood
Open
Large stems (>5-cm DBH)
Stem size
Small stems (<5-cm DBH)
Stems/0.05 ha
(b) Steam density
Figure 2: Mean overhead canopy cover (a) and mean stem density (b) for hardwood (gray bars) and open (white bars) cover types. Error bars
represent 95% confidence intervals.
flock directions was when flocks moved quickly across
boundaries (Figure 3(c)).
3.3. Within-Flock Movements. We were able to observe and
record the movement response of birds to the initial move-
ment of 113 focal individuals (focal species; including 3
observations of nonflocking species) across the 20 flocks
observed. The flocking type of the focal species observed
(nuclear, satellite, or nonflocking) was independent of
whether or not the responding individual was conspecific or
heterospecific (G=1.4, df =2, P=0.5). This suggests that
responding individuals did not only respond to conspecific
focal individuals.
Overall, a responding individual’s directionality of move-
ment within the flock was more highly correlated with satel-
lite focal individuals than it was with TUTI focal individuals
(Table 2). For movement through different cover types,
angular-angular correlations (raa) between the movement
direction of focal individuals and responding individuals
showed that in hardwoods and more open habitats, a re-
sponding species was more likely to move in the same direc-
tion as a TUTI than a satellite species; however, at bound-
aries, a responding individual’s movement direction was very
highly correlated with the movement direction of satellite
focal individuals (Table 2).
When considering within-flock movements for the two
different movement distance classes (<15 m versus >15 m),
when focal individuals moved less than fifteen meters,
a responding individual’s movement direction was more cor-
related with the movement direction of satellite focal indi-
viduals and this was also the case for movement through
open cover types (Table 2). In open habitat, there was
a significant negative correlation between the within-flock
movement direction of TUTI and responding individuals. In
contrast, the correlation between the movement directions of
TUTI and responding individuals was significantly greater in
hardwood cover (Table 2).
For within-flock movements where focal individuals
moved >15 m, a responding individual’s movement direction
was more correlated with satellite movements for all habitats
combined (Table 2). At boundaries, correlations were greater
when focal individuals were satellite species (there was no
significant correlation for focal TUTI), but for open cover
types, the correlation was greater when focal individuals were
TUTI. In hardwood cover, there was no significant correla-
tion for the focal TUTI, but there was a significant negative
correlation with focal satellite species movement directions
(Table 2).
4. Discussion
4.1. Flock Leadership by Titmice Suggests a Passive Nuclear
Role. As we predicted, the movement directions of TUTI
were clearly more highly correlated with overall flock paths
than with the movement directions of satellite species
participating in the same flock (Figure 3(a)), supporting our
hypothesis that TUTI are followed by satellites in mixed-
species flocks (e.g., TUTI act as a passive nuclear species).
This was particularly obvious when flocks were moving
fast and moving across boundaries between hardwood and
open cover types (Figures 3(a) and 3(c)). When flocks were
moving slowly, however, correlations were less consistent
in open and boundary cover but were consistent with our
predictions in hardwood habitat (Figure 3(b)). Since mean
flock movement rates were greater across boundaries than
mean flock movement rates in open or forest cover types,
perhaps the most parsimonious explanation for the loss of
TUTI leadership in slow-moving flocks in open habitat is
that vegetative substrate for perching in that cover type was
sparser than in the subcanopy of hardwood forests, providing
fewer options for an individual to use as a destination perch
during flock-following (Figure 2). Even when flocks are
stalled in hardwood habitat that is dominated by large, multi-
branching oaks, each flock participant will be surrounded

International Journal of Zoology 7
0
0.05
0.1
0.15
0.2
0.25
0.3
All cover Boundary Hardwood Open
Cover types
raa
N=113
N=13
N=60
N=36
N=24
N=233
N=67
N=29
(a) All flock movement rates
−0.15
−0.05
0.05
0.15
0.25
0.35
0.45
All cover Boundary Hardwood Open
Cover types
raa
N=49
N=69
N=29
N=12
N=7
N=110 N=29
N=13
(b) Slow flock movement rate (<30 m/5 minutes)
0
0.05
0.1
0.15
0.2
0.25
0.3
0.35
0.4
All cover Boundary Hardwood Open
Cover types
Nuclear
Satellite
N=64
N=61
N=31
N=24
N=17
N=123
N=38
N=16
raa
(c) Fast flock movement rate (>30 m/5 minutes)
Figure 3: Angular-angular correlation coefficients (raa) for correlations between the movement direction of nuclear (TUTI; gray bars) or
satellite (white) flock participants and flock movement direction in all cover types combined (All Cover), boundary (boundary between
hardwood and open cover), hardwood, and open cover types. The sample size for each coefficient is above each bar. (a) Correlation
coefficients in different cover types for all flock movement rates; (b) Correlation coefficients in different cover types for slow flock movement
rates (<30 m/5 minutes); (c) Correlation coefficients in different cover types for fast flock movement rates (>30 m/5 minutes). Error bars
represent 95% confidence intervals for each raa. Missing error bars represent 95% confidence intervals that were too small to be visible (CI <
0.001).
by high densities of potential perching substrates. Thus,
individuals seeking to stay close to TUTI can always move
in the direction of a TUTI individual in hardwood forest and
have a suitable perch in a preferred location. In an open pine
habitat, however, perching and foraging substrate and cover
availability will all be much sparser overall. Therefore, if the
TUTI are not moving then movements of individuals seeking
to stay in the area with TUTI will be influenced more by
feeding or other activities which, if perches are limited, may
take them away from TUTI or closer to other satellite species
(Figure 3(b)). Indeed, given (a) the dominant assumption
that more open habitats convey higher predation risk for
small birds in general [9,34,38], and (b) that TUTI may
be especially targeted by predators attacking flocks (T. A.
Contreras and K. E. Sieving, unpublished data, see above),
avoidance of stalled TUTI by flock mates in open habitats
may be prudent (Figure 3(b)). However, these variations
on our central prediction do not detract from the overall
conclusion that when foraging flocks are moving, TUTI
movements define the flock path in all wooded habitats that
we studied. The only way that this pattern could reflect other
than purely passive leadership on the part of the nuclear
species is if TUTI were somehow compelling other species
to follow or rally around them. Given that titmouse (and
other parid) mobbing calls do indeed attract a high variety of
species [20,39], rallying calls directed at heterospecifics are
quite possible. However, such calls are as yet undocumented
despite extensive examination of parid vocal repertoires
[40]; their detection was beyond our capabilities in this
study.

8International Journal of Zoology
Tab l e 2: Angular-Angular correlation coefficients (raa) for correlations between a focal individual’s movement direction and the movement
direction of responding individuals (within-flock movement) in different cover types and for different movement distances of focal
individuals. N=number of individuals observed. Confidence intervals (95% CI) for each raa are reported (L1,L2;seeZar[35]). Confidence
intervals that do not include 0 indicate a significant raa (in bold print) at P<0.05.
Overall Cover type
(All cover types) Boundary Hardwood Open
Flock role raa N95% CI (L1,L
2)raa N95% CI (L1,L
2)raa N95% CI (L1,L
2)raa N95% CI (L1,L
2)
All focal individuals
Nuclear 0.101 65 0.097, 0.101 −0.072 16 −0.101, −0.078 0.170 29 0.163, 0.174 0.267 20 0.257, 0.279
Satellite 0.182 45 0.181, 0.187 0.918 5 0.880, 0.953 0.049 28 0.046, 0.062 0.197 12 0.169, 0.234
Focal individual <15 m
Nuclear 0.034 34 0.024, 0.033 −0.094 9 −0.070, 0.004 0.173 18 0.151, 0.179 −0.243 7−0.315, −0.140
Satellite 0.121 25 0.116, 0.129 N/A 1 N/A 0.063 19 0.056, 0.074 0.328 5 0.140, 0.650
Focal individual >15 m
Nuclear 0.207 31 0.201, 0.211 0.037 7 −0.041, 0.087 −0.025 11 −0.063, 0.024 0.393 13 0.369, 0.406
Satellite 0.339 20 0.339, 0.354 0.986 4 0.983, 0.996 −0.168 9−0.182, −0.109 0.160 7 0.070, 0.303
4.2. Within-Flock Movement Patterns May Reflect Social Com-
plexity within Flocks. We detected a great variety of patterns
with respect to fine-scale movements of satellite and nuclear
species (Table 2), and almost no corroboration of our central
prediction of high correlations between TUTI movements
and subsequent satellite movements. As mentioned above,
this could be due to the rapidly shifting and complex
social environment within mixed-species flocks that likely
dominates participants’ attention simultaneously with avoid-
ing predators and searching for food. Increasing evidence
suggests that while mixed-species foraging flocks may have
evolved under selection to avoid predators while enhancing
foraging efficiency (reviewed in Sridhar et al. [10]), once
formed, flocks will host a wide variety of other behaviors
that are equally critical to survival and reproduction. Within
the permanent bird flocks that are characteristic of tropical
forests (canopy, understory, and ant following), the life cycles
of flock participants play out within an intensely social
environment [41–43]. While engaged in facultative winter
flocks, temperate forest resident and migrant birds experi-
ence a similarly complex social milieu including (in addition
to antipredator vigilance and foraging) everything from
information gathering [44,45], mate assessment and status
signaling [46], territorial defense [47], courtship [48], to a
complex variety of conspecific and heterospecific dominance
interactions and competitive conflicts over food and feeding
sites [49–51]. Thus, the finding that fine-scale movements
of birds in mixed flocks are not predictable based on
a single factor (spatial cohesion with the nuclear species). For
example, 3 of the satellite species most frequently observed
in flocks (Carolina Chickadee, Ruby-crowned Kinglet, Pine
Warbler; Table 1) have foraging behaviors similar to those
of TUTI (e.g., lower canopy/shrub foragers or gleaners; De
Graaf et al. [52]) and are subordinate to TUTI. Given TUTI’s
propensity to steal food, it is not surprising that satellite
species often move away from TUTI when approached
within 5 meters (Table 2).
While their aggression, vigilance, and gregariousness
make TUTI excellent community informants [19,53], mob
leaders [9,20], and nuclear species in foraging flocks [1,4],
these same traits likely reduce their attractiveness at close
distances. In our experience with keeping TUTI in aviaries
[54], we find TUTI can be exceptionally aggressive toward
unfamiliar individuals in confined spaces. Our data also
suggest that satellite species are more willing to tolerate each
other at close range than are TUTI (Table 2). The only high
correlation between satellite and TUTI movement directions
in our analysis occurred when movement distances were
greater than 15 m in open cover types. At these distances, we
are seeing movements that are more closely related to overall
flock movement; the kinds of movements that satellites
should be tracking in order to “keep up” with flocks. Both
of our analyses suggest that the nuclear-satellite species
relationships and social roles are indeed context dependent
[12], influenced by habitat type (and associated perception
of predation risk), habitat structure, flock speed, movement
distances made by individuals, and spatial scales over which
movements occur (e.g., within vs. between foraging patch
and across habitat boundaries).
Therefore, our results suggest that within slow-moving
flocks, individuals may be responding to the movement of
other individuals in the flock and less attention may be
paid to nuclear species. Conversely, as flocks move greater
distances, and relatively faster through landscapes, TUTI
act as flock leaders and passive nuclear species, particularly
in cover types that may be perceived as more hostile by
forest passerines, for example, open cover types and while
crossing forest-open cover type boundaries; see Sieving
et al. [9]. Srinivasan et al. [12] suggested that for mixed-
species aggregations, acting as a nuclear species may not
be a “fixed species property”, that is, species characteristics
that determine species suitability as a nuclear species, or
even as flock leaders, may be “context dependent”. Het-
erospecific interactions and the roles of mixed-species flock
members may change as flocks move through landscapes
and different cover types. Traits that would make TUTI
suitable as flock leaders and nuclear species (e.g., socially
dominant/aggressive, generalized habitat use, and high vocal

International Journal of Zoology 9
complexity; [4,19,20]) when flocks are moving quickly or
moving long distances through potentially dangerous cover
types may not make them the preferred attractant (e.g.,
passive nuclear species) for other flocking species as flocks
engage in other activities while flocking.
5. Conservation Implications
Our findings contribute to an expanding base of information
suggesting that parids serve as community-level facilitators
of (potentially) a great number of heterospecifics in diverse
taxa. Because parids tend to be very common where they
occur, designating them as “keystone facilitators” is not
technically correct (their effect on flock dynamics and com-
munity structure is not disproportionate to their abundance;
[55]). Moreover, we can eliminate “mutualism” from our
descriptions, because the observed passive leadership of
flocks by TUTI further underscores the probable lack of fit-
ness benefits for TUTI in mixed species flocks. Nonetheless,
the facilitative effects of titmice and parids are likely to be
pervasive in Holarctic woodland bird communities. Tufted
titmice and other parids are habitat generalists, that are able
to exploit wood and shrub lands with varied species compo-
sition and habitat structures, but species that associate with
them are often more specialized in habitat use [56]. Given
that spatial behavior can limit the functional connectivity of
fragmented and degraded forest landscapes for vertebrates
(see Crooks and Sanjayan [57]), nuclear species with broad
niches and less sensitivity to changes in physical connectivity
may greatly enhance flock movement and increase access
to spatially constrained resources for satellites willing to
follow them. For example, tufted titmice clearly expand
the foraging niches of their winter satellites [7], and they
increase the permeability of high contrast habitat boundaries
to satellite movement [8,9,58]. Thus, following titmice may
largely counteract the strong effects of lethal and nonlethal
predation threats that constrain movement and access to
resources [18,59] for flock associates. Paridae include a high
proportion of nuclear species and/or flock leaders [14]and
traits that support the role of nuclear species in mixed flocks
are well developed and conserved across the family, including
high vocal complexity [19], bold personality [60], and high
vigilance [61,62]. Therefore, across the Holarctic, it is likely
that parid-led mixed-species flocks gain similar foraging and
habitat exploitation advantages on their winter home ranges.
Parid facilitation of other species is not limited to mixed
flocks. Heterospecific attraction has been defined as the
deliberate selection of breeding territories by migrants that
are already populated by resident heterospecifics [26,27].
Heterospecific attraction is strong between parids (as the
resident attractor) and migrant forest passerines that
breed sympatrically with them (experimental documenta-
tion comes from Scandinavian and North American parid
species; [24,60]). The positive benefits of using resident
parids as cues for settlement are especially pronounced
in high latitudes, where short nesting seasons make rapid
identification of productive breeding habitat critical for long-
distance migrants [63,64]. Additionally, enhanced repro-
ductive success may accrue to heterospecifics from nesting
near parids [65]. Thus, attraction of heterospecifics to parids
occurs across scales, from foraging microhabitat to choice of
breeding patch, and it enhances fitness-related measures at
the level of individuals and alters species distributions within
communities. Thus, our work with flocks leads us to concur
with current thinking that facilitation is as important (or
more so) as competition and predation in shaping selective
regimes and species patterns within animal communities
[66].
One clear benefit that heterospecifics gain by being close
enough to parids to hear them is the exceptionally high-
quality information parids produce that precisely and accu-
rately conveys their perception of predation risks and threats
[19,21,22,67]. Changes in the types of titmouse calls as
they move through the landscape may reflect changes in their
perception of predation risk [19]. Therefore, it would be
beneficial for any species that share predators with titmice
to be able to interpret and respond appropriately to titmouse
calls. Moreover, the number and diversity of species across
the Holarctic that utilize parid information to inform their
predator-avoidance decisions are apparently very large [20,
53,68]. Thus, we argue that the facilitative role of parids may
best be described as “community informants.” The use of
socially derived information from parids to effectively avoid
predators enables heterospecifics to achieve greater efficiency
in other critical activities and provides a largely sufficient
explanation for heterospecific attraction to parids, both
within winter flocks or breeding bird communities [46,69].
Therefore, we view the most important implication of our
work as this: in attempts to conserve declining species that
may be receiving important benefits from association with
parids, consideration should be given to maintaining or
strengthening those benefits in conservation strategies.
Acknowledgments
The authors would like to thank Marcela Machicote, Stacia
Hetrick, and other members of the K. E. Sieving lab for their
comments on the initial design of this study. Two anonymous
reviewers provided valuable comments and suggestions on
previous drafts of this paper. They thank the Department
of Wildlife Ecology and Conservation at the University of
Florida for allowing us to work at the Ordway-Swisher
Biological Station and also to the Florida Department of
Environmental Protection for granting permission to con-
duct parts of the study at the San Felasco Hammock Preserve
and the Payne’s Prairie Preserve State Parks. Their study was
funded by an NSF Postdoctoral Fellowship to T. A. Contreras
(DBI no. 0309753).
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