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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? 1 2 Thomas A. Contreras and Kathryn E. Sieving Biology Department, Washington and Jeﬀerson College, 60 S. Lincoln Street, Washington, PA 15301, USA Department 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 to be followed by satellites, but active nuclear species are still able to maintain ﬂock cohesion (see review in Farley et al. Multispecies bird ﬂocks, comprising individuals that move ). A variety of ﬁtness beneﬁts can accrue to satellite species together in organized association with each other as they for- as a result of ﬂocking with nuclear species, but beneﬁts to age during daylight hours, are a common phenomenon in nuclear species are less obvious [7–12]. forested ecosystems of the world . Flock participants Parids (family Paridae) function as nuclear species in occupy diﬀerent behavioral niches, or social roles, within winter and nonbreeding mixed-species forest ﬂocks in North ﬂocks. Flocking species are generally classiﬁed into “nuclear” America and elsewhere in the Holarctic [4, 7–9, 13]. As a and “satellite” roles [2–4]. Nuclear species are those ﬂock family, parids have traits that predispose them to nuclear participants whose conspicuous behaviors (distinctive alarm roles in heterospeciﬁc groups; they are intraspeciﬁcally social or other vocalizations and active movements) enhance ﬂock [1, 14, 15] and aggressive mobbers of potential predators, cohesion and may stimulate ﬂock formation. Nuclear species usually leading mobbing events; their behavior may signiﬁ- are typically intraspeciﬁcally social (occurring in extended cantly reduce predation risk for satellite species [4, 11, 13, 14, family groups for some of the year), and they occur more 16–19]. In the Eastern United States of America, the tufted often in ﬂocks than outside of them when ﬂocks occur [5, 6]. titmouse (TUTI; Baeolophus bicolor) is a socially dominant Nuclear species are thought to fall into two general catego- parid that functions as a nuclear species in ﬂocks even where ries : passive or active nuclear species [2, 3]. Passive nuclearity TUTI co-occur with chickadees in ﬂocks (chickadees may is hypothesized to come about when satellite species actively also serve as nuclear species when not participating in ﬂocks seek out and follow the nuclear species, thereby deﬁning the with TUTI ). TUTI, like other parids, produce copious nuclear species as the ﬂock leader. Conversely, active nuclear threat-related vocalizations that are thought to be signals species are hypothesized to seek out and join existing mixed- meant for conspeciﬁcs but that are used as informational species ﬂocks and are just as likely to follow the satellites as cues by numerous heterospeciﬁcs [19–22]. Some parids give 2 International Journal of Zoology food-related cues for conspeciﬁcs , but their use by het- Studies in North-Central Florida [4, 9, 16, 17] and else- erospeciﬁcs has not been documented to our knowledge. where in Eastern NA (see Greenberg ) identify TUTI as the primary nuclear species in most winter mixed-species Thus, the central known ﬁtness beneﬁts available to satel- bird ﬂocks. While this classiﬁcation of TUTI is based on lite species, or heterospeciﬁc associates of parids more gener- their pervasive presence in winter foraging ﬂocks and their ally, may be the reduction of predation risk during critical dominating role in mixed-species mobbing ﬂocks [7, 9], the activities [9, 19]. Dolby and Grubb Jr.  demonstrated that question remains whether TUTI are functioning as passive when TUTI were removed from isolated woodlots, individu- or active nuclear species in winter foraging ﬂocks. Accord- als of satellite species remaining in those woodlots in winter ingly, we used a correlative analysis of TUTI and satellite occupied reduced foraging niches, avoided exposed foraging movements at two spatial scales of ﬂocking behavior which sites, and declined in overall physical condition relative to we categorized as: (1) the correlation between the movement individuals who were in woodlots where TUTI had not of TUTI or satellites with overall ﬂock movement through been removed. The presence of parids enhances access to a landscape (ﬂock leadership) and (2) the correlation between resources and microhabitats within forest bird home ranges the movement of TUTI or satellites with the movement of (; aids heterospeciﬁcs in ﬁnding suitable breeding habitat immediate ﬂock members (within-ﬂock movement). via heterospeciﬁc attraction; ) and possibly increases We followed mixed-species ﬂocks during a single winter nest success . These ﬁndings suggest that the prodigious (2004) in North-Central Florida, mapping the overall move- amount of information that parids produce concerning their ment directions of ﬂocks and the movement directions of immediate perceptions of predation risk aids their fellow randomly selected satellite species and TUTI in each ﬂock prey species in many aspects of decision making including (providing comparisons for both analyses; ﬂock leadership, (a) increased foraging eﬃciency, (b) access to critical micro- and within-ﬂock movements). Based on Farley et al. , we and macrohabitats, and (c) an elevation of the eﬀectiveness classiﬁed individuals in the ﬂock as nuclear species (TUTI), of antipredator defense [10, 19, 22, 25, 26]. satellite species (species who are “regular and occasional Determination of whether nuclear species interact with associates” in mixed-species ﬂocks), or nonﬂocking species. heterospeciﬁcs passively or actively in mixed ﬂocks has only If TUTI are functioning as passive nuclear species and ﬂock received speculation at this point , yet this kind of infor- leaders, then we predicted that (1) overall ﬂock movement mation could enhance understanding of the evolutionary direction should be more highly correlated with the move- ecology of facilitation, parasitism, and mutualism in animal ment direction of individual TUTI than with those of satellite communities . For example, if titmice are active nuclear species (Figure 1(a)) and (2) the within-ﬂock movement species, soliciting close relationships with other species, it directions of satellite species in ﬂocks should be more highly would suggest that they accrue beneﬁts from associated correlated with the movement direction of the nearest TUTI heterospeciﬁcs . In thiscase, it mightbeproductiveto than with the nearest satellite species (Figure 1(b)). test whether the ﬁnely tuned antipredator calls of tufted Previous observations of forest bird mobbing activity titmice may involve active signaling to heterospeciﬁcs rather (see Sieving et al. ) also suggest that satellite species may be than being purely intraspeciﬁc (kin) signals that are gleaned more likely to move through areas with less vegetative cover by eavesdropping heterospeciﬁcs . If,however,titmice (open cover types) when TUTI are present, especially when are passive ﬂock leaders being followed by other species, then perceived or actual risk of predation may be high. There- exploring aspects of heterospeciﬁc exploitation of the nuclear fore, we also predicted stronger correlations between TUTI species would be most productive . To date, we have movement direction and ﬂock movement direction as ﬂocks conﬂicting evidence regarding what tufted titmice may gain move through more open cover types. in the presence of heterospeciﬁcs. One potential beneﬁt is food items taken from smaller satellites (kleptoparasitism; 2. Materials and Methods ). However, we have witnessed that the only species in actively foraging mixed ﬂocks that reliably get killed during 2.1. Study System. To test our predictions, we observed and hawk attacks are titmice (T. A. Contreras and K. E. Sieving, followed wintering mixed-species: forest passerine ﬂocks in unpublished data), suggesting that the presence of ﬂocks may North-Central Florida from January to March, 2004. Flocks be an important ﬁtness cost to titmice. Here, we sought were observed at 3 sites: (1) the University of Florida’s to determine whether TUTI are passive or active nuclear Ordway-Swisher Biological Station (Putnam County; N ◦ ◦ species in order to inform future research questions and 29 41 45.6 ,W81 58 56.2 ), (2) the San Felasco Ham- critically assess the common assumption that mixed-species mock Preserve State Park (Alachua County; N 29 42 46.3 , bird ﬂocks are models of mutualism . If satellite and W82 27 23.7 ), and (3) Payne’s Prairie Preserve State Park nuclear species are not gaining ﬁtness through association, (Bolen’s Bluﬀ location; Alachua County; N 29 33 24.6 , then it would be more productive to assume that the W82 19 47.5 ). All 3 sites had similar vegetation and full range of exploitative (parasitic and commensal) and cover types. In hardwood stands (cover type: hardwood), mutualistic relationships are displayed in ﬂocks [10, 27, 31]. the canopy and subcanopy layers were dominated primarily We undertook an analysis to distinguish active from passive by laurel oak (Quercus laurifolia), live oak (Q. virginiana), ﬂock leadership by TUTI in order to clarify future steps in sand live oak (Q. geminata), water oak (Q. nigra), pignut understanding the ecological and evolutionary relationships hickory (Carla glabra), sweetgum (Liquidambar styraciﬂua), acting within mixed species ﬂocks. or cabbage palm (Sabal palmetto), while the understory was International Journal of Zoology 3 Responding bird Focal bird Satellite species S 2 Species 2 Species 1 TUTI (a) Hypothesized movement paths (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 T , T , T ,and T representing estimated 0 1 2 3 ﬂock centers at 0, 5, 10, and 15 minutes respectively. Lines S , S ,and S represent “movement” segments between estimated ﬂock centers, 1 2 3 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 2.2.1. Flock Leadership Data. We collected data for determin- (Serenoa repens). More open habitats (cover type: open) used ing ﬂock leadership at 5-minute intervals, and during each in the study generally had a sparse overstory of widely dis- interval, we (1) estimated and marked the center of the ﬂock persed mature longleaf pine (Pinus palustris) with a patchily (based on the area of the aggregation with the greatest esti- distributed subcanopy of Quercus spp. (primarily turkey oak mated number of birds) by placing a wire ﬂag in the ground, (Quercus laevis) and sand live oak), and rosemary (Ceratiola (2) identiﬁed the ﬂocking species and estimated the number ericoides), and understory dominated by wiregrass (Aristrida of individuals present in the ﬂock, and (3) estimated the stricta), exotic grasses, saw palmetto, and various forms. movement azimuth (degrees), of multiple randomly selected Flocks occurred throughout the woodland communities of TUTI and satellite focal individuals at each ﬂock center our study areas, and we sought replicate samples in 3 (azimuths of sampled individuals were estimated from the major cover types that were identiﬁed as (a) hardwood and ﬂock center using a compass; Figure 1(b)). If we lost track of (b) pine-dominated (open) forest and (c) the boundaries a ﬂock during the observation period, we then searched for between these two major forest classiﬁcations. Indeed, ﬂock anew ﬂock to observe. dynamics varied across these three habit designations, and 2.2.2. Within-Flock Movement Data. During each 5-minute we included them as predictors in our analyses (see below). interval, we estimated the direction and distance of move- 2.2. Flock Observations and Data Collection. Mixed-species ments made by randomly selected individuals in the ﬂock ﬂocks without TUTI are rarely observed in our study region and of the next movement made by another ﬂock participant ; therefore, we systematically searched each of the 3 study that was closest to the ﬁrst bird, assuming that the “respond- areas for the presence of TUTI using existing trails and roads, ing individual” was moving in response to the movement of and then initiated observations of the associated ﬂocks. the focal individual. These estimates were used for determin- To reduce the possibility of pseudoreplication of individual ing within-ﬂock movement correlations (Figure 1(b)). To and ﬂock movement data, we never surveyed any speciﬁc maximize the potential that the responding bird was actually area more than once and each ﬂock observed was at least responding to, or aware of, the focal bird’s movement, the 350 m from any other ﬂocks observed, based on maximum second bird had to be within 5 m of the focal bird’s initial reported TUTI winter home range sizes [17, 32]. Once lo- position and had to move within 60 seconds of the focal cated, ﬂocks were followed for a minimum of 15 minutes, bird’s movement; otherwise, we selected a new focal bird and allowing birds to become acclimated to the observer (T. A. responding individual. And if, within a ﬂock, we lost track of Contreras in all cases). Flocks were considered acclimated individuals under observation, we selected a new focal bird when birds stopped approaching the observer, and alarm and responding individual. calls were infrequent or directed at other bird species. After To randomly select individuals for observations (both acclimation, we followed the ﬂock for a maximum of 55 “ﬂock leadership” and “within ﬂock movement”), at each minutes. ﬂock center, we started at a randomly selected azimuth and 4 International Journal of Zoology then scanned the ﬂock in a clockwise direction for the ﬁrst ily follow TUTI and not each other. First, we asked which focal individual that moved more than 5 m horizontally. We species are leading/directing the path of the ﬂock (ﬂock lead- then estimated the movement distance (using a range-ﬁnder) ership) by testing whether TUTI movement paths (direction and the movement direction (azimuth) of that individual. of movements during 5 min intervals) are more highly cor- The azimuth for each individual was estimated from the related with the overall ﬂock paths than with satellite species initial point where the individual was observed. In some movement directions). Second, we tested whether individual cases, this often meant marking the initial and subsequent satellite species were tracking the ﬁne-scale movements of horizontal positions with pin ﬂags and then returning later nearby titmice more so than those of nearby satellite species to obtain measurements. Although individuals within ﬂocks (within-ﬂock movements). For all analyses we used α = 0.05 were not marked and could have been observed more than to determine statistical signiﬁcance. once within each ﬂock, randomizing the selection of ﬂock members for observations, and the relatively large number 2.3.1. Flock Leadership. Using movement data for both ﬂocks of individuals per ﬂock may has reduced the probability and individuals for each 5-minute time segment, we ﬁrst cal- of pseudoreplication of observations of individual ﬂock culated correlation coeﬃcients between the azimuth for ﬂock participants. movement during each of the 5-minute time intervals and the azimuth for randomly selected individuals in the ﬂock 2.2.3. Characterization of Flock Path and Habitat. After ob- during the 5-min interval. We divided analyses between servations were completed for each ﬂock, we determined the the three cover type classes where ﬂocks were observed overall path of each ﬂock. We returned to the ﬁrst ﬂock center (hardwood, open (pine), or boundary), and for this analysis observed (which had been ﬂagged) and measured its position included further subdivisions of the data into two ﬂock using a global positioning system (GPS, accuracy ±3m; movement distance categories (fast, >30 m/5 minutes; slow, Garmin GPSMap 76, Garmin International Inc., Olathe, <30 m/5 minutes). This latter categorization was adopted, Kan, USA). The distance and direction (azimuth) of each because ﬂock movement rates varied greatly around the subsequent ﬂock center relative to the previous ﬂock center mean of 30 m/5 min; some ﬂocks were sometimes stalled, was measured using a compass and range ﬁnder and then whereas at other times a ﬂock could move up to 131 m/5 min plotted by connecting lines between successive ﬂock centers (see Section 2.2. Flock Observations and Data Collection), (Figure 1(b)). Distances between ﬂock centers ranged from and we noted that movement dynamics appeared to diﬀer 0–131 m with a mean distance of 32 ± 21 m (±SD). between relatively slow and fast-moving ﬂocks. Finally, analyses were further subdivided by ﬂock role (nuclear At each of the ﬂock centers, we recorded the “cover type” (TUTI) vs. satellite species; Table 1). that the ﬂock and individuals moved through (for each 5-min segment of movement): (1) hardwood, (2) open (gen- 2.3.2. Within-Flock Movements. To test the prediction that erally pine sandhill or other pine stands with sparse canopy the within-ﬂock movement direction and distance of indi- cover), and (3) boundary, for example, the ﬂock crossed vidual ﬂock members would be more highly correlated with the boundary between hardwood and pine cover types those of the nuclear species (TUTI), we calculated correlation during a 5-minute segment. Using the GPS to ﬁnd the coeﬃcients (r ) and associated 95% conﬁdence intervals approximate position of the ﬁrst ﬂock center allowed us to aa between the movement azimuths of randomly selected indi- plot the overall path using a GIS (ArcView v3.2, ESRI, viduals within the ﬂock (focal species) and the ﬁrst individ- Redlands, Calif, USA) to view ﬂock centers overlaid on digital ual to move after the focal individual moved (responding orthophoto quarter-quadrangles with 1-m resolution (1999; species). As above, the data were subdivided by focal species Land Boundary Information System (LABINS), Florida type (i.e., nuclear (TUTI) versus satellite species; nonﬂocking Dept. of Environmental Protection, Bureau of Survey and species were not included in this analysis) and cover type. We Mapping, Tallahassee, Fla, USA) and conﬁrm cover types for further subdivided the analyses by the movement distance of each subsequent ﬂock center. In addition, within a 0.05-ha focal species using two distance classes: individuals moved circle surrounding each estimated ﬂock center, we estimated <15 m or >15 m. These distance classes for within-ﬂock (1)the proportionsofoverheadcanopy(e.g.,emergent, movement are based on the mean within-ﬂock movement of dominant, and codominant crown classes) and subcanopy focal species (15.5±21 m (±SD)), and were delineated to rep- cover using a densitometer, (2) the density of large stems resent biologically reasonable distinctions between exploita- >5-cm diameter at breast height (DBH) using the point- tion of a single foraging patch (within 15 m) versus changing quarter method , and (3) the number of small stems foraging patches (moving more than 15 m in a single move- <5-cm DBH but >1 m in height within the 0.05-ha circle. ment). Only movements >5 m were recorded/analyzed, since We predicted that there would be signiﬁcant diﬀerences movements of less than 5 m were very frequent and probably between hardwood and open cover types in one or more correlated with movements of escaping prey rather than ﬂock of the vegetation characteristics, and this might help inform mates. our interpretations of movement patterns; that is, birds may If only conspeciﬁcs are responding to focal individu- move faster or slower through more open habitats, and this als, then correlations of within-ﬂock movement directions can inﬂuence ﬂock cohesion . between focal and responding individuals would suggest that 2.3. Data Analysis. Two spatial scales of movements were the movement of individuals within ﬂocks was inﬂuenced analyzed to assess the prediction that satellite species primar- primarily by intraspeciﬁc interactions. Therefore, we used International Journal of Zoology 5 Table 1: All species encountered in mixed-species ﬂocks during the diﬀerent. If CI’s for correlation coeﬃcients (in general), and study (classiﬁed into ﬂock roles (nuclear, satellite, or nonﬂocking) for other directional measures similar to r ’s, do not overlap, aa based on Farley et al. ). Percentage of ﬂocks is the percentage of and if the CI’s are similar in magnitude, then meaningful the 20 ﬂocks where the species was encountered at a minimum of diﬀerences can safely be assumed (see Nakagawa and Cuthill one observation point. Max. number of individuals is the estimated  for discussion). maximum number of individuals in a ﬂock observed at one time. %ofﬂocks/max. 3. Results Common name Scientiﬁc name # of individuals 3.1. Flock Observations. In total, 20 ﬂocks were observed at Nuclear our study sites (13 ﬂocks at the Ordway-Swisher Preserve, 5 Tufted titmouse Baeolophus bicolor 100/6 ﬂocks at the San Felasco Hammock Preserve State Park, and Satellite 2 ﬂocks at the Payne’s Prairie Preserve State Park) with an Black-and-white warbler Mniotilta varia 50/2 average of 8 ﬂock centers mapped per ﬂock path recorded Blue-gray gnatcatcher Polioptila caerulea 70/6 (range = 4–12 ﬂock centers). There was a signiﬁcant dif- Blue-headed vireo Vireo solitarius 30/2 ference in ﬂock movement rates (per segment) in diﬀerent Carolina chickadee Poecile carolinensis 20/3 cover types (F = 7.56, P = 0.0007, r = 0.10). Flock 2,131 movement rates were signiﬁcantly greater as ﬂocks crossed Downy woodpecker Picoides pubescens 40/3 boundaries (12.5± 4.0m/minute (±SD)) when compared to Dendroica (Yellow) palm warbler 15/15 movement rates of ﬂocks in hardwood (6.1 ± 4.5m/minute palmarum (±SD)) or open (6.1 ± 3.5m/minute (±SD)) cover types. Pine warbler Dendroica pinus 35/2 A total of 16 species were detected, and besides TUTI, only Melanerpes Red-bellied woodpecker 30/3 two others were present in the majority of ﬂocks observed: carolinus Ruby-crowned Kinglets and Blue-gray Gnatcatchers which Ruby-crowned kinglet Regulus calendula 95/15 were present in 95% and 70% of the ﬂocks, respectively White-eyed vireo Vireo griseus 15/1 (Table 1). Mean species richness for the 20 ﬂocks was 5.6 ± Dendroica 1.7 species per ﬂock (±SD) with a mean maximum number Yellow-throated warbler 10/1 dominica of individuals in each ﬂock of 23.8 ± 23.2 individuals (±SD). Nonﬂocking Five common species observed in or near ﬂock centers, that are not ﬂock participants (nonﬂocking species, Farley Blue jay Cyanocitta cristata 5/3 et al. ; Table 1), were excluded from all analyses except Eastern bluebird Sialia sialis 5/2 for the G-test above. Along ﬂock paths, the proportion of Yellow-rumped warbler Dendroica coronata 15/50+ overhead canopy cover was greater in hardwood than in Northern parula Parula americana 10/2 open (pine) cover types (Figure 2(a)), whereas proportions Zonotrchia White-throated sparrow 5/20 of overhead subcanopy, small stem density, and large stem albicollis 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 a G-test of independence to determine if there was a lack of independence between the movement of the focal species two general habitat types, subcanopy and shrub cover is similar. 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 3.2. Flock Leadership. We observed a total of 346 individuals focal species (nuclear vs. satellite vs. nonﬂocking species) and (113 TUTI and 233 satellites) whose movement directions the rows being whether or not the responding species was a were correlated with ﬂock movement at 117 ﬂock centers. For conspeciﬁc or heterospeciﬁc. Cells within the table contained all cover types (slow and fast-moving ﬂocks pooled) and for the frequency of responding individuals. both slow and fast-moving ﬂocks (cover types pooled), ﬂock Since correlation coeﬃcients for circular data (e.g., movement direction was more highly correlated with the azimuths) should not be calculated using statistical tests movement direction of TUTI than with the movement direc- for linear measurements , we used Igor Pro statistical tion of satellites (Figures 3(a), 3(b),and 3(c)). When ﬂocks software (v.6.2.1, Wavemetrics, Inc., Lake Oswego, Ore, USA) were moving slowly across boundaries, satellite movement to calculate Angular-Angular correlation coeﬃcients (r ), direction and ﬂock movement direction were more highly aa which are analogous to a Pearson’s r (see methods described correlated, whereas in open (pine) cover there was a negative in Zar  and Fisher ) and the 95% conﬁdence intervals correlation between ﬂock and TUTI movement directions associated with each r . If “0” did not fall within the con- (Figure 3(b)). We note relatively small sample sizes for the aa ﬁdence interval calculated for an r , then the correlation latter two ﬁndings (Figure 3(b)). For fast-moving ﬂocks aa coeﬃcient was statistically signiﬁcant at P< 0.05 . Given (>30 m/5 minutes; Figure 3(c)), the movement direction of the lack of signiﬁcance testing options for angular correla- TUTI was more highly correlated with ﬂock movement di- tions (we found none), we relied on the 95% conﬁdence rection than with the movement direction of satellite species intervals (CI) for each r to make inferences about whether in all cover types. The greatest diﬀerence between correlation aa or not r ’s from comparable categories were biologically coeﬃcients calculated for TUTI and satellite species with aa 6 International Journal of Zoology 0.9 0.8 160 0.7 0.6 0.5 100 0.4 80 0.3 0.2 40 0.1 20 0 0 Large stems (>5-cm DBH) Small stems (<5-cm DBH) Canopy Subcanopy Stem size Vegetation layer Hardwood Hardwood Open Open (a) Proportion overhead cover (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 For within-ﬂock movements where focal individuals boundaries (Figure 3(c)). moved >15 m, a responding individual’s movement direction was more correlated with satellite movements for all habitats 3.3. Within-Flock Movements. We were able to observe and combined (Table 2). At boundaries, correlations were greater record the movement response of birds to the initial move- when focal individuals were satellite species (there was no ment of 113 focal individuals (focal species; including 3 signiﬁcant correlation for focal TUTI), but for open cover observations of nonﬂocking species) across the 20 ﬂocks types, the correlation was greater when focal individuals were observed. The ﬂocking type of the focal species observed TUTI. In hardwood cover, there was no signiﬁcant correla- (nuclear, satellite, or nonﬂocking) was independent of tion for the focal TUTI, but there was a signiﬁcant negative whether or not the responding individual was conspeciﬁc or correlation with focal satellite species movement directions heterospeciﬁc (G = 1.4, df = 2, P = 0.5). This suggests that (Table 2). responding individuals did not only respond to conspeciﬁc focal individuals. 4. Discussion Overall, a responding individual’s directionality of move- ment within the ﬂock was more highly correlated with satel- 4.1. Flock Leadership by Titmice Suggests a Passive Nuclear lite focal individuals than it was with TUTI focal individuals Role. As we predicted, the movement directions of TUTI (Table 2). For movement through diﬀerent cover types, were clearly more highly correlated with overall ﬂock paths angular-angular correlations (r ) between the movement than with the movement directions of satellite species aa direction of focal individuals and responding individuals participating in the same ﬂock (Figure 3(a)), supporting our showed that in hardwoods and more open habitats, a re- hypothesis that TUTI are followed by satellites in mixed- sponding species was more likely to move in the same direc- species ﬂocks (e.g., TUTI act as a passive nuclear species). tion as a TUTI than a satellite species; however, at bound- This was particularly obvious when ﬂocks were moving aries, a responding individual’s movement direction was very fast and moving across boundaries between hardwood and highly correlated with the movement direction of satellite open cover types (Figures 3(a) and 3(c)). When ﬂocks were focal individuals (Table 2). moving slowly, however, correlations were less consistent When considering within-ﬂock movements for the two in open and boundary cover but were consistent with our diﬀerent movement distance classes (<15 m versus >15 m), predictions in hardwood habitat (Figure 3(b)). Since mean when focal individuals moved less than ﬁfteen meters, ﬂock movement rates were greater across boundaries than a responding individual’s movement direction was more cor- mean ﬂock movement rates in open or forest cover types, related with the movement direction of satellite focal indi- perhaps the most parsimonious explanation for the loss of viduals and this was also the case for movement through TUTI leadership in slow-moving ﬂocks in open habitat is open cover types (Table 2). In open habitat, there was that vegetative substrate for perching in that cover type was a signiﬁcant negative correlation between the within-ﬂock sparser than in the subcanopy of hardwood forests, providing movement direction of TUTI and responding individuals. In fewer options for an individual to use as a destination perch contrast, the correlation between the movement directions of during ﬂock-following (Figure 2). Even when ﬂocks are TUTI and responding individuals was signiﬁcantly greater in stalled in hardwood habitat that is dominated by large, multi- hardwood cover (Table 2). branching oaks, each ﬂock participant will be surrounded Proportion overhead cover Stems/0.05 ha International Journal of Zoology 7 N = 12 0.45 0.3 N = 24 0.35 0.25 N = 113 N = 29 N = 60 N = 7 0.25 0.2 N = 67 N = 29 0.15 N = 49 0.15 N = 233 N = 13 N = 36 N = 110 0.05 N = 29 N = 69 0.1 −0.05 0.05 −0.15 N = 13 All cover Boundary Hardwood Open All cover Boundary Hardwood Open Cover types Cover types (a) All ﬂock movement rates (b) Slow ﬂock movement rate (<30 m/5 minutes) N = 16 0.4 N = 31 0.35 N = 64 N = 38 N = 61 0.3 0.25 N = 17 N = 123 0.2 0.15 0.1 0.05 N = 24 All cover Boundary Hardwood Open Cover types Nuclear Satellite (c) Fast ﬂock movement rate (>30 m/5 minutes) Figure 3: Angular-angular correlation coeﬃcients (r ) for correlations between the movement direction of nuclear (TUTI; gray bars) or aa 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 r . Missing error bars represent 95% conﬁdence intervals that were too small to be visible (CI < aa 0.001). by high densities of potential perching substrates. Thus, avoidance of stalled TUTI by ﬂock mates in open habitats individuals seeking to stay close to TUTI can always move may be prudent (Figure 3(b)). However, these variations in the direction of a TUTI individual in hardwood forest and on our central prediction do not detract from the overall have a suitable perch in a preferred location. In an open pine conclusion that when foraging ﬂocks are moving, TUTI habitat, however, perching and foraging substrate and cover movements deﬁne the ﬂock path in all wooded habitats that availability will all be much sparser overall. Therefore, if the we studied. The only way that this pattern could reﬂect other TUTI are not moving then movements of individuals seeking than purely passive leadership on the part of the nuclear to stay in the area with TUTI will be inﬂuenced more by species is if TUTI were somehow compelling other species feeding or other activities which, if perches are limited, may to follow or rally around them. Given that titmouse (and take them away from TUTI or closer to other satellite species other parid) mobbing calls do indeed attract a high variety of (Figure 3(b)). Indeed, given (a) the dominant assumption species [20, 39], rallying calls directed at heterospeciﬁcs are that more open habitats convey higher predation risk for quite possible. However, such calls are as yet undocumented small birds in general [9, 34, 38], and (b) that TUTI may despite extensive examination of parid vocal repertoires be especially targeted by predators attacking ﬂocks (T. A. ; their detection was beyond our capabilities in this Contreras and K. E. Sieving, unpublished data, see above), study. aa aa aa 8 International Journal of Zoology Table 2: Angular-Angular correlation coeﬃcients (r ) for correlations between a focal individual’s movement direction and the movement aa 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 r are reported (L , L ;see Zar). Conﬁdence aa 1 2 intervals that do not include 0 indicate a signiﬁcant r (in bold print) at P < 0.05. aa Overall Cover type (All cover types) Boundary Hardwood Open Flock role r N 95% CI (L ,L ) r N 95% CI (L ,L ) r N 95% CI (L ,L ) r N 95% CI (L ,L ) aa 1 2 aa 1 2 aa 1 2 aa 1 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- leaders [9, 20], and nuclear species in foraging ﬂocks [1, 4], plexity within Flocks. We detected a great variety of patterns these same traits likely reduce their attractiveness at close with respect to ﬁne-scale movements of satellite and nuclear distances. In our experience with keeping TUTI in aviaries species (Table 2), and almost no corroboration of our central , we ﬁnd TUTI can be exceptionally aggressive toward prediction of high correlations between TUTI movements unfamiliar individuals in conﬁned spaces. Our data also and subsequent satellite movements. As mentioned above, suggest that satellite species are more willing to tolerate each this could be due to the rapidly shifting and complex other at close range than are TUTI (Table 2). The only high social environment within mixed-species ﬂocks that likely correlation between satellite and TUTI movement directions dominates participants’ attention simultaneously with avoid- in our analysis occurred when movement distances were ing predators and searching for food. Increasing evidence greater than 15 m in open cover types. At these distances, we suggests that while mixed-species foraging ﬂocks may have are seeing movements that are more closely related to overall evolved under selection to avoid predators while enhancing ﬂock movement; the kinds of movements that satellites foraging eﬃciency (reviewed in Sridhar et al. ), once should be tracking in order to “keep up” with ﬂocks. Both formed, ﬂocks will host a wide variety of other behaviors of our analyses suggest that the nuclear-satellite species that are equally critical to survival and reproduction. Within relationships and social roles are indeed context dependent the permanent bird ﬂocks that are characteristic of tropical , inﬂuenced by habitat type (and associated perception forests (canopy, understory, and ant following), the life cycles of predation risk), habitat structure, ﬂock speed, movement of ﬂock participants play out within an intensely social distances made by individuals, and spatial scales over which environment [41–43]. While engaged in facultative winter movements occur (e.g., within vs. between foraging patch ﬂocks, temperate forest resident and migrant birds experi- and across habitat boundaries). ence a similarly complex social milieu including (in addition Therefore, our results suggest that within slow-moving to antipredator vigilance and foraging) everything from ﬂocks, individuals may be responding to the movement of information gathering [44, 45], mate assessment and status other individuals in the ﬂock and less attention may be signaling , territorial defense , courtship , to a paid to nuclear species. Conversely, as ﬂocks move greater complex variety of conspeciﬁc and heterospeciﬁc dominance distances, and relatively faster through landscapes, TUTI interactions and competitive conﬂicts over food and feeding act as ﬂock leaders and passive nuclear species, particularly sites [49–51]. Thus, the ﬁnding that ﬁne-scale movements in cover types that may be perceived as more hostile by of birds in mixed ﬂocks are not predictable based on forest passerines, for example, open cover types and while a single factor (spatial cohesion with the nuclear species). For crossing forest-open cover type boundaries; see Sieving example, 3 of the satellite species most frequently observed et al. . Srinivasan et al.  suggested that for mixed- in ﬂocks (Carolina Chickadee, Ruby-crowned Kinglet, Pine species aggregations, acting as a nuclear species may not Warbler; Table 1) have foraging behaviors similar to those be a “ﬁxed species property”, that is, species characteristics of TUTI (e.g., lower canopy/shrub foragers or gleaners; De that determine species suitability as a nuclear species, or Graaf et al. ) and are subordinate to TUTI. Given TUTI’s even as ﬂock leaders, may be “context dependent”. Het- propensity to steal food, it is not surprising that satellite erospeciﬁc interactions and the roles of mixed-species ﬂock species often move away from TUTI when approached members may change as ﬂocks move through landscapes within 5 meters (Table 2). and diﬀerent cover types. Traits that would make TUTI While their aggression, vigilance, and gregariousness suitable as ﬂock leaders and nuclear species (e.g., socially make TUTI excellent community informants [19, 53], mob dominant/aggressive, generalized habitat use, and high vocal International Journal of Zoology 9 complexity; [4, 19, 20]) when ﬂocks are moving quickly or near parids . Thus, attraction of heterospeciﬁcs to parids moving long distances through potentially dangerous cover occurs across scales, from foraging microhabitat to choice of types may not make them the preferred attractant (e.g., breeding patch, and it enhances ﬁtness-related measures at passive nuclear species) for other ﬂocking species as ﬂocks the level of individuals and alters species distributions within engage in other activities while ﬂocking. 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 5. Conservation Implications regimes and species patterns within animal communities . Our ﬁndings contribute to an expanding base of information suggesting that parids serve as community-level facilitators One clear beneﬁt that heterospeciﬁcs gain by being close of (potentially) a great number of heterospeciﬁcs in diverse enough to parids to hear them is the exceptionally high- taxa. Because parids tend to be very common where they quality information parids produce that precisely and accu- occur, designating them as “keystone facilitators” is not rately conveys their perception of predation risks and threats technically correct (their eﬀect on ﬂock dynamics and com- [19, 21, 22, 67]. Changes in the types of titmouse calls as munity structure is not disproportionate to their abundance; they move through the landscape may reﬂect changes in their ). Moreover, we can eliminate “mutualism” from our perception of predation risk . Therefore, it would be beneﬁcial for any species that share predators with titmice descriptions, because the observed passive leadership of ﬂocks by TUTI further underscores the probable lack of ﬁt- to be able to interpret and respond appropriately to titmouse ness beneﬁts for TUTI in mixed species ﬂocks. Nonetheless, calls. Moreover, the number and diversity of species across the Holarctic that utilize parid information to inform their the facilitative eﬀects of titmice and parids are likely to be pervasive in Holarctic woodland bird communities. Tufted predator-avoidance decisions are apparently very large [20, titmice and other parids are habitat generalists, that are able 53, 68]. Thus, we argue that the facilitative role of parids may to exploit wood and shrub lands with varied species compo- best be described as “community informants.” The use of sition and habitat structures, but species that associate with socially derived information from parids to eﬀectively avoid predators enables heterospeciﬁcs to achieve greater eﬃciency them are often more specialized in habitat use . Given that spatial behavior can limit the functional connectivity of in other critical activities and provides a largely suﬃcient fragmented and degraded forest landscapes for vertebrates explanation for heterospeciﬁc attraction to parids, both within winter ﬂocks or breeding bird communities [46, 69]. (see Crooks and Sanjayan ), nuclear species with broad niches and less sensitivity to changes in physical connectivity Therefore, we view the most important implication of our may greatly enhance ﬂock movement and increase access work as this: in attempts to conserve declining species that to spatially constrained resources for satellites willing to may be receiving important beneﬁts from association with follow them. For example, tufted titmice clearly expand parids, consideration should be given to maintaining or the foraging niches of their winter satellites , and they strengthening those beneﬁts in conservation strategies. increase the permeability of high contrast habitat boundaries to satellite movement [8, 9, 58]. Thus, following titmice may Acknowledgments largely counteract the strong eﬀects of lethal and nonlethal predation threats that constrain movement and access to The authors would like to thank Marcela Machicote, Stacia resources [18, 59] for ﬂock associates. Paridae include a high Hetrick, and other members of the K. E. Sieving lab for their proportion of nuclear species and/or ﬂock leaders and comments on the initial design of this study. Two anonymous traits that support the role of nuclear species in mixed ﬂocks reviewers provided valuable comments and suggestions on are well developed and conserved across the family, including previous drafts of this paper. They thank the Department high vocal complexity , bold personality , and high of Wildlife Ecology and Conservation at the University of vigilance [61, 62]. Therefore, across the Holarctic, it is likely Florida for allowing us to work at the Ordway-Swisher that parid-led mixed-species ﬂocks gain similar foraging and Biological Station and also to the Florida Department of habitat exploitation advantages on their winter home ranges. Environmental Protection for granting permission to con- Parid facilitation of other species is not limited to mixed duct parts of the study at the San Felasco Hammock Preserve ﬂocks. Heterospeciﬁc attraction has been deﬁned as the and the Payne’s Prairie Preserve State Parks. Their study was deliberate selection of breeding territories by migrants that funded by an NSF Postdoctoral Fellowship to T. A. Contreras are already populated by resident heterospeciﬁcs [26, 27]. (DBI no. 0309753). Heterospeciﬁc attraction is strong between parids (as the resident attractor) and migrant forest passerines that References breed sympatrically with them (experimental documenta- tion comes from Scandinavian and North American parid  R. Greenberg, “Birds of many feathers: the formation and species; [24, 60]). 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