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

Leadership of Winter Mixed-Species Flocks by Tufted Titmice (Baeolophus bicolor): Are Titmice... 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 [4]). 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 [1]. 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 [14]). 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 [23], 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 [1]) 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. [7] 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 ([9]; aids heterospecifics in finding suitable breeding habitat immediate flock members (within-flock movement). via heterospecific attraction; [24]) and possibly increases We followed mixed-species flocks during a single winter nest success [25]. 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. [4], 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 [10], 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 [27]. 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 [28]. 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. [9]) 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 [15]. 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 [10]. 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 [29]). 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 [30]. 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 [4]; 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 [33], 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 [34]. 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. [4]). 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 [37] 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. [4]; 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 [35], 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 [35] and Fisher [36]) 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 [35]. 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. [40]; 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[35]). 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 [54], 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. [10]), 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 [12], 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 [46], territorial defense [47], courtship [48], 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. [9]. Srinivasan et al. [12] 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. [52]) 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 [65]. 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 [66]. 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 [55]). Moreover, we can eliminate “mutualism” from our perception of predation risk [19]. 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 [56]. 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 [57]), 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 [7], 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 [14]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 [19], bold personality [60], 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). 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Leadership of Winter Mixed-Species Flocks by Tufted Titmice (Baeolophus bicolor): Are Titmice Passive Nuclear Species?

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Copyright © 2011 Thomas A. Contreras and Kathryn 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.
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Abstract

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 [4]). 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 [1]. 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 [14]). 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 [23], 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 [1]) 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. [7] 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 ([9]; aids heterospecifics in finding suitable breeding habitat immediate flock members (within-flock movement). via heterospecific attraction; [24]) and possibly increases We followed mixed-species flocks during a single winter nest success [25]. 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. [4], 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 [10], 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 [27]. 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 [28]. 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. [9]) 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 [15]. 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 [10]. 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 [29]). 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 [30]. 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 [4]; 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 [33], 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 [34]. 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. [4]). 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 [37] 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. [4]; 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 [35], 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 [35] and Fisher [36]) 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 [35]. 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. [40]; 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[35]). 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 [54], 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. [10]), 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 [12], 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 [46], territorial defense [47], courtship [48], 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. [9]. Srinivasan et al. [12] 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. [52]) 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 [65]. 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 [66]. 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 [55]). Moreover, we can eliminate “mutualism” from our perception of predation risk [19]. 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 [56]. 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 [57]), 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 [7], 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 [14]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 [19], bold personality [60], 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). 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