Mate Protection and Winter Pair-Bonds in Black-Capped Chickadees ’

The Condor 99~424-433 0 The Cooper Ormthological Society 1997

MATE PROTECTION AND WINTER PAIR-BONDS IN BLACK-CAPPED CHICKADEES ’

DAVID LEMMON Department of Biological Sciences, Universini at Albany, SUNY, Albany, NY 12222, e-mail: dl0296@&bm.albany.eda

MATTHEW L. WITHIAM Childrens’ Hospital of Buffalo, Department of Gynecology and Obstetrics, 219 Bryant St., BufSalo, NY 14210

CHRISTOPHER I? L. BARKAN Research & Test Department, Environmental and Hazardous Materials Division, Association of American Railroads, 50 F Street NW, Washington, D.C. 20001-1564

Abstract. Black-cappedChickadees (Parus atricupillus) that bred together in the spring had significantly higher winter associationindices than birds that did not breed together, indicating winter pairing. Most members of winter flocks were paired, and pair members had the same within-sex dominance rank in nine out of ten cases.These resultsconfirm the findings of other studiesof wintering chickadees.We report the first quantified example of mate protectionin a North American parid. From observationsof chickadeesvisiting feeders in winter, we identified three benefits for females paired to alpha males that are consistent with the hypothesis of mate protection: (1) these females were subject to less intense aggression from their mate, compared with that between other dominants and subordinates. When accompaniedby their mate, these females experienced (2) less frequent aggression and (3) maintaineda higher feeding rate than other subordinatesin the presenceof dominant flock members. Chickadeescommonly form a “pair-hierarchy” within a flock. We suggest that mate protection has a role in the formation of pair-hierarchies,and that mate protection is the main cause of the overlap in survival rates between the sexes. These results,and this view, suggestthat a wintering female’s pair bond status may have a greater effect on her fitness than her dominance rank. Key words: Black-capped Chickadee, dominance rank, mate protection, Parus atricapillus, winter association indices, winter pair-bonds.

INTRODUCTION Work on a European parid, the Willow Tit Pair bonding in birds has been described pri- (Parus montunz~s),has identified some immedi- marily in the context of the breeding season ate benefits of winter pair-bonds to females. In (Emlen and Oring 1977, Wittenberger 1979, Willow Tit flocks, males usually are dominant Wittenberger and Tilson 1980). Until recently, to females (Hogstad 1987b), and winter survival less attention has been paid to pair bonds (i.e., is closely related to an individual’s dominance close associations) during the nonbreeding sea- rank within its sex (Koivula and Ore111988, Ek- son. Winter pair-bonding has been demonstrated man 1990). Nevertheless, female Willow Tits in Black-capped Chickadees (Parus atricapillus) paired to dominant males survive the winter bet- (Ficken et al. 1981, Smith 1984, 1990), and ter than some subordinate males that rank above Smith (1984) has shown that members of the them (Ekman 1984, Hogstad 1989, Ekman highest-ranked chickadee pair of a flock survive 1990). This probably comes about through mate the winter better and are more likely to obtain a protection. Dominant males appear to protect breeding territory than members of lower-ranked their mates from aggressive encounters and ex- pairs (also see Desrocherset al. 1988). However, posure to predators by excluding other flock the immediate costs and benefits of the winter members from preferred foraging areas (Ekman pair-bond to each sex, and the nature of the in- and Eskenmo 1984, Hogstad 1988, Ekman 1990, fluence of dominance rank, remain to be exam- Koivula et al. 1994). Protected females show ined. lower vigilance rates (Ekman 1990, Hogstad 1992) and higher feeding rates (Hogstad 1992) ’ Received 4 January 1996. Accepted 20 November than other subordinates. Dominant males also 1996. may directly protect their mates from predators

14241 MATE PROTECTION IN CHICKADEES 425 by alarm calling. When presented with a model bany County, New York. We captured chicka- predator, a dominant male Willow Tit was more dees during the fall and winter and marked each likely to give an alarm call if its mate was near- bird with a unique combination of colored leg by (Hogstad 1995). bands to allow the identification of individuals. Mate protection has not been demonstratedin Wingchord length and details of skull ossifica- North American parids. Smith (1991) cites an tion were taken at the time of banding. We at- unpublished study by J. A. Leak (1986) which tached coded flagging tape to trees at regular describes circumstantial evidence of mate pro- intervals throughout the study area to serve as tection (different levels of male aggression to- landmarks. The study area was surveyed and a ward old and young females), but other causes scale map constructed,enabling us to plot sight- could not be ruled out. In the present study, we ings of chickadees with 10 m accuracy. examine the behavior of pair bonded Black-cap- We made observations of social dominance ped Chickadees in winter and evaluate evidence interactions and feeding behavior at feeders con- of mate protection. taming small amounts of sunflower seed frag- Wintering chickadees form hocks of up to ments. This was the only time supplemental twelve unrelated individuals, but more common- food was provided. Food was available only for ly six to ten (Smith 1991). Within a flock there a short period on any given day and was never is a linear dominance hierarchy in which males available when association data were collected. are nearly always dominant to females (Glase Providing food in this way probably had little 1973, Smith 1976), and winter survival is close- effect on the chickadees’ long-term use of space ly linked to dominance rank within a sex (Smith or associationpatterns. Additionally, landowners 1984, 1994, Desrochers et al. 1988). Yet, like near Byron Wood agreed not to set up feeders Willow Tits, females paired to dominant males for the duration of the study. survive the winter better than some subordinate males (Smith 1984). If female survival is linked FLOCK COMPOSITION to mate protection, then mate protection might Chickadees were considered members of a flock be expected to occur in Black-capped Chicka- if they had high association indices (see below) dees. and similar home-range centers (Withiam and Dominance interactions can be potentially Barkan, unpubl. data). We also use the term costly in terms of energy and injury, and can group for a collection of chickadees, and this is determine access to preferred foraging sites. not used synonymously with flock. A group was Thus, the frequency, intensity and effectiveness a temporary assemblage of chickadees, which of dominance interactions are likely to influence could comprise all or some members of one the relative survival rate of flock members, flock, or members from several flocks. probably largely through their effects on foraging time (Ekman 1990). For example, the level ASSOCIATION INDICES of aggression experienced by a flock member Chickadees found within 20 m of one another affects its feeding rate (Hogstad 1992). If mate were considered associates.We calculated an as- protection operates in chickadees, we predict sociation index (coincidence index of Dice that: (1) an alpha male’s level of aggression to- 1945) for all combinations of birds within each ward his mate would be less than that between of six flocks (ranging in size from three to eight other dominants and subordinates, (2) a female individuals) using the formula: accompanied by her alpha mate would be sub- Association index = 2W(A + B), ject to fewer aggressiveinteractions, and (3) she would maintain a higher feeding rate than other where: H = the number of sightings in which subordinates in the presence of dominant flock individuals a and b were considered associates, members. Predictions (2) and (3) are similar to A = the total number of sightings of bird a, and those of Hogstad (1992). B = the total number of sightings of bird b. An association index of 1.0 indicates that birds a METHODS and b were always seen as associates,and an STUDY AREA index of 0.0 indicates that birds a and b were The study was conducted at Byron Wood, a never seen as associates. 90-ha mixed forest located in Guilderland, Al- To minimize any site-dependent bias in esti- 426 DAVID LEMMON ET AL. mating association indices, we allocated equal During the winters of 1983/1984 and 1984/1985, search effort to each hectare of the study area. the collection of dominance data continued until In the winter of 1983/1984, each hectare was each dyad in a flock showed a statistically sig- systematically searchedfive times for a total of nificant dominance relationship using a binomial 100 (? 15) min. In the winter of 1984/1985 each test. During the winter of 1985/1986, a complete hectare was systematically searchedfive to eight record of dominance relationships and home times for a total of 110 (+ 5) min. All searches range use patterns was not collected. However, were made between January and March, with we did obtain significant dominance relation- similar search efforts in each month. When ships for all birds used in the estimates of feed- chickadees were sighted, we recorded their lo- ing rate (see below). cation and associations.To assure statistical in- Four types of aggressiveinteraction were used dependence of sightings, we never followed a to determine dominance relationships: (1) chase; chickadee group after an encounter. The same the winner chased the loser away from the feed- group of chickadees rarely was encountered er with overt aggressive behavior (e.g., calling, more than once in a particular search. For those wing displays), (2) supplant; the winner dis- that were, we considered them independent placed the loser from the feeder with overt ag- sightings only if they were separated by more gressive behavior, (3) avoid; the winner dis- than 10 min. Over 98% of all sightings were placed the loser without overt aggressivebehav- separatedby one hour or more. ior, and (4) wait; the winner occupied the feeder while the loser waited nearby (< 3 m); the loser BREEDING PAIRS gained accessto the feeder only after the winner We establishedthe identity of breeding pairs, be- left. These criteria are similar to those used in tween April &June 30, in several ways. The other studies of chickadee dominance relation- most important of these was the response of ships (e.g., Dixon 1965, Glase 1973). In our pairs to a tape recording of the chickadee’s “fee- analyses, these four dominance criteria were bee” song, played systematically throughout the separated into two categories, active (1 and 2) study area. To be classified as a breeding pair, and passive (3 and 4). Active interactions often the same two birds had to respond to the re- entailed the aggressor approaching within 1 m cording on at least five different days during the of the loser and sometimes resulted in physical breeding season.The bird that sang when a pair contact. We therefore assumed that active dom- arrived at the tape player was assumed to be inance interactions were more costly energeti- male (Ficken et al. 1978, Weise 1979). Pair iden- cally and more likely to result in injury than tity was further confirmed from independent passive interactions. sightings of the male presenting food to the female (Orr and Verbeek 1981). Pairs responded FEEDING RATE to recordings at a particular site on the study Individuals were observed from nine flocks, area in a manner consistent with the defense of ranging in size from five to eight members. We territories, and incidental sightings of pairs al- estimated the feeding rate of individuals in ways occurred in the same areas in which they groups of one to three from film records of their originally responded to the recordings. The sex behavior at a specialized feeder. The feeder was of individuals was established from breeding a small elevated cup fitted with a cardboardcol- pair information and winter dominance rank. lar to narrow the opening, and contained small Age was determined from skull ossification pat- fragments of sunflower seeds of a standardized terns in the fall. size. The cup was secured to a pole at a height of about 1.4 m and positioned within the home SOCIAL DOMINANCE range of each flock in areas with similar A chickadee’s dominance rank within its flock amounts of cover. This placement of the feeder was determined by recording the winners and controlled for the effects of feeder height (Len- losers of aggressiveinteractions at a feeder and drem 1983) and distance to cover (Caraco et al. entering the outcomes into dominance matrices 1980) on the time an individual might spend using the method of Brown (1975). The domi- scanning for predators.By observing only small nance hierarchy of a Parus flock does not groups, the importance of a central or peripheral change at feeders (Smith 1976, Hogstad 198713). position in a flock on predator-scanningbehavior MATE PROTECTION IN CHICKADEES 427

also was minimized (Hamilton 1971, Jennings male mates (birds that bred together the follow- and Evans 1980). ing spring), (b) male-female nonmates (birds We characterizedthe social context for an in- that did not breed togetherthe following spring), dividual’s visit to the feeder in terms of group (c) male-male, and (d) female-female. The mean size (the number of birds within 10 m of the associationindex for each of the four association feeder), and the presence or absence of more categories is shown in Figure 1. We tested for dominant birds in the group (see below). We significantly different means using Duncan’s filmed feeder visits with a Bell and Howell Su- multiple range test for unequal sample sizes per 8 camera. We attempted to film a bird on (Milton and Tsokos 1983) with arcsine trans- the feeder for at least 20 set, but no more than formed data. Males and females that bred to- 30 set, to minimize effects of satiation. For the gether had a significantly higher mean associa- same reason, birds were not filmed once they tion index the previous winter than all other as- had accumulated more than 60 set of feeder- sociation categories (P < 0.01 for all compari- time during a flocks visit to the feeder. Filming sons). The mean associationindices of the other was ended early if a bird was displaced (most three categoriesdid not differ significantly from common occurrence), group size changed (in- one another (P > 0.05 for all comparisons). eluding a change because another speciesjoined These data indicate the existence of winter pair- the flock), or an alarm call was given. Repeat bonds in Black-capped Chickadees. filming of a flock was separatedby at least two Chickadee pair bonding appeared to take hours. We did not limit filming with respect to place mostly in the fall, during the onset of flock time of day or temperature. Feeder visits were formation. Some first-year birds were pair bond- filmed at a distance of 20-30 m, without a blind, ed in winter, and some adults were paired with but in a position partially obscured by vegeta- birds other than those with whom they had bred tion. A bird visiting the feeder could either peck the previous summer. However, pair bonds also for food (have its head below the rim of the could form in midwinter. In two instances, birds cup), or it could scan (have its head above the that were from different flocks in early winter rim of the cup). When taking food, its vision were later found in the same flock with associ- was completely obscuredby the cardboardcollar ation indices typical of pair bonded birds. Both and walls of the cup. Hence, pecking and scan- pairs bred the following spring. These patterns ning were alternating and mutually exclusive be- of pairing are consistent with those generally haviors and were easily observable on film dur- found in chickadees (Smith 1991). ing a frame-by-frame analysis. Using an identical feeder in a laboratory set- BREEDING STATUS ting, we found a linear relationship between Over the course of the study, 20 of the 27 birds peck rate and food consumption; that is, no cor- for which winter association indices were ob- relation was found between peck duration (the tained bred the following summer. In all cases, time an individual had its head below the rim of the members of a breeding pair had been mem- the cup) and the mass of food taken (rs = bers of the same flock the preceding winter. In -0.143, P > 0.05, n = 50). Thus, feeding rate nine out of the ten breeding pairs, the male and was estimated as the mean of the inverse of the female had the same within-sex dominance rank; sum of a peck and subsequentscan duration, or that is, alpha males bred with alpha females, pecks set-‘. Feeding rates were log transformed beta males bred with beta females, and so on. to achieve normal distributions; therefore, geo- This is commonly the case (Smith 1991). metric means are reported. We compared feed- INTENSITY OF DOMINANCE INTERACTIONS ing rates within each group size using independent-sample two-tailed r-tests. We found a clear dominance-subordinance relationship for all dyads in the dominance matrix RESULTS for each flock. In all flocks, individuals could be ranked in a linear hierarchy within which all ASSOCIATION INDICES males were dominant to all females. This is the We obtained association indices for all combi- usual pattern (Glase 1973), but exceptions can nations of two birds within a winter flock. There occur (Smith 1991). were four association categories: (a) male-fe- The mean proportion of active dominance in- 428 DAVID LEMMON ET AL.

c ‘2 0.6 - :: 1 g 0.4 -

S 0.2 -

0.0 -

6*&? cr*s9 d&a” 989 (M) NJ)

Association Category FIGURE 1. Mean associationindices (t 2 SE) for wintering Black-capped Chickadees in each association category. Male-female associationsare separatedinto birds that were mated (M) or unmated (U) the following spring. Bars are standarderrors, line through bar is mean, and numbers above bars are sample sizes. Means connectedby lines do not differ significantly (P > 0.05, Duncan’s multiple range test). teractions for each associationcategory is shown for all other associationcategories (P < 0.05 for in Figure 2. We compared means using Duncan’s all comparisons). The means of the remaining multiple range test for unequal sample sizes with three association categories did not differ sig- arcsine transformed data. The mean proportion nificantly from one another (P > 0.05 for all of active dominance interactions between pair comparisons). These results support prediction bonded birds was significantly lower than that 1: an alpha male’s level of aggressiontoward his

g l.O- g : 4 0.8- 5 $ .r:5 0.6- E B $ 0.4 - S‘ 2 IO

,E 0.2 - :: f o.o-

Association Category

FIGURE 2. Mean proportion of active dominance interactions(5 2 SE) between wintering chickadeesin each associationcategory. (M) and (U) are the same as in Figure 1. Numbers above bars are sample sizes. Means connectedby lines do not differ significantly (P > 0.05, Duncan’s multiple range test).

430 DAVID LEMMON ET AL. higher feeding rate than subordinatesin a group chide data from birds foraging naturally and vis- of two and a 43% higher feeding rate in a group iting feeders. of three. These results support prediction 3: a The benefits to females demonstrated in our female accompanied by her alpha mate main- study cannot be explained by atypical domi- tains a higher feeding rate than other subordinance relationships; as noted, all males were nates in the presence of dominant flock mem- dominant to all females. Neither can our results bers. be explained by males and females being less Recall that feeding rate (pecks secl) is the aggressivetoward one another generally, regard- mean of the inverse of the sum of a peck and less of the pair bond. The proportion of active subsequent scan duration. Mean peck duration dominance interactions between nonpaired for females paired to alphas and for subordinates males and females was significantly higher than did not vary significantly within each group- the proportion between paired birds (Fig. 2). Al- size, whereas mean scanning duration was sig- though we do not have an estimate of feeding nificantly shorterfor paired females in groups of rate for females that were not pair bonded, these two and three (unpubl. data). Therefore, the dif- females did experience a higher proportion of ferences in feeding rate when dominants were active dominance interactions than paired fe- present (groups of two and three) was due to males (unpubl. data). Because the level of ag- paired females spending less time scanning than gression a chickadee experiences is a good in- subordinates.That is, paired females had a high- dicator of its feeding rate (Fig. 3) unpaired fe- er feeding rate because they had a shorter inter- males probably had a lower feeding rate than val between pecks. These differences in feeding females accompanied by their mates, especially rate can be attributed to dominance effects, and those accompanied by alpha males. not group-size effects, because comparisons The finding that a female accompanied by her were made within a group-size. The higher feed- alpha mate receives less aggression than other ing rate of paired females cannot be explained subordinatesin a group is not solely a result of by their holding a higher dominance rank than reduced aggression by her mate. On several oc- the subordinates; on the contrary, 78% of the casions, we witnessed the supplanter of a female subordinate feeding rate data were for males, paired to alpha being immediately chasedby al- which rank above females. pha (cf. Ekman 1990). The data on feeding rate (Fig. 3) suggest that such protection forms the DISCUSSION larger part of the pair bond benefit. Consider the feeding rate of a female paired to alpha in a We have confirmed Ficken et al. (1981) and group of three. If reduced aggression by alpha Smith’s (1984, 1990) findings that Black-capped was the sole benefit, these females would be ex- Chickadeesare commonly pair bonded in winter, pected at best to maintain a feeding rate com- and that members of a pair are often matched in parable to a subordinate in a group of two. That dominance rank (Smith 1991). Pairs that bred is, the effect of the presence of the two domi- together were found togetherin winter over 80% nants on a paired female’s feeding rate in a of the time, compared with 40% to 50% for the group of three could be discounted by one dom- other association categories. We identified three inant (her mate). But these females have an el- immediate benefits of the pair bond for females evated feeding rate compared with a subordinate accompanied by their alpha mate: compared in a group of two--and the difference can be with other subordinatesin the presence of dom- attributed to the presence of alpha. This com- inants, these females experienced (1) less in- parison is not confounded by a positive effect of tense aggression from a dominant-their mate, group-size on the feeding rate of subordinates, (2) less frequent aggression, and (3) a higher because subordinate feeding rate drops across feeding rate as a result of less time spent scan- groups of one to three (Fig. 3). ning for aggressors.These results represent the The benefits of mate protection for females first quantified example of mate protection in a appear to operate in the short-term through an North American parid. Wintering female Willow influence on survival. From patterns of induced Tits paired to alpha males derive the same ben- feather growth (indicating nutritional condition) efits we documented for chickadees (Ekman among flock members, Hogstad (1992) demon- 1990, Hogstad 1992). The Willow Tit studiesin- strated that mate protection is probably directly MATE PROTECTION IN CHICKADEES 431 responsible for an enhanced nutritional condi- (Hogstad 1988, Ekman 1990, Hogstad 1992), tion of female Willow Tits paired to alphas. that by improving the survival chances and Mate protection appearsto influence directly the overwinter condition of his mate, the male im- amount of food available to these females proves his chances of having a mate in the through alpha excluding subordinatesfrom pre- spring, breeding early and producing surviving ferred foraging sites (Ekman and Askenmo young. 1984, Hogstad 1988, Ekman 1990) and foraging Mate protection benefits also should accrue to close to his mate (Hogstad 1992). Under these pairs of a lower rank than alpha. Females paired circumstances, paired females reduce their vig- to beta males in the present study appeared to ilance for potential aggressorsand thereby in- experience less aggression than expected (un- crease the time available for foraging (Ekman publ. data) and this should translate into a higher 1990, Hogstad 1992). There also is some release feeding rate. Beta male Willow Tits appear to from vigilance for predators at preferred sites adopt the same predator-warning behavior as al- (Ekman 1987). Becausewinter survival in parids phas in regard to their mates (Hogstad 1995). can be directly linked to food availability (Jann- Because members of chickadee pairs usually son et al. 1981, Desrochers et al. 1988) and its match in rank (alpha with alpha, beta with beta, effect on exposure to predators (Jannson et al. etc.), Smith (1991) suggestedthat the structure 1981), Hogstad’s (1992) work provides a strong of a chickadee flock might be seen more usefully link between mate protection and the survival of as one of a hierarchy of pairs rather than one of paired females. individuals. Hogstad (1987b) and Ekman (1990) For males, benefits of mate protection are viewed Willow Tit flocks as comprising subunits probably delayed, while costs (from dominant of pairs matching in rank. Mate protection may behavior) are incurred immediately. Maintaining have a role in this pattern of pairing. Several alpha status is costly metabolically (Roskaft et factors (e.g., age, size) affect a female’s domi- al. 1986, Hogstad 1987a), and there are potential nance rank (Smith 1991), but the effect of her injury costs associatedwith dominance interac- mate’s rank and associatedprotection behavior tions and predator-alarm behavior. In contrast to may supersedeother factors that ordinarily de- females, the benefits of mate protection for termine her rank. There are examples of young males seem to be deferred until the following female chickadees being dominant to older fe- breeding season. Female parids generally sur- males when the young birds are paired with al- vive the winter less well than their mates (e.g., pha males (e.g., Glase 1973, Ficken et al. 1990). Ekman 1990), although in Black-capped Chick- In Willow Tits, Hogstad (1987b) showed that the adees this appears not to be so until after their rank of juvenile females correlated with that of first breeding attempt (Smith 1994). For male their mate, regardless of the body size of the Willow Tits, the loss of a mate could result in females. Moreover, Hogstad found that the rank the loss of a breeding season (potential mates of a juvenile female could be lowered by the are scarce due to male-biased sex ratios in the removal of her mate. Through its influence on spring [Ekman 19901). Male chickadees do not female rank, male mate protection may thus in- face the same problem of replacing a mate fluence the pairing pattern. The effect of mate (Smith 1991), but finding a replacement or a protection on rank usually would be limited to mate in poor condition could delay the start of just the female hierarchy because male and fe- breeding (S. Smith, pers. comm.). In Willow male ranks do not overlap as a rule. Exceptions Tits, the timing of the start of breeding, and thus to this ranking (when a female is dominant to a the timing of dispersal of young, is important in male) often involve age differences, but not al- determining dominance rank (and thereby sur- ways (Smith 1991), and in either situation mate vival) of young in their first winter (Hogstad protection could still play a role. 1987b, 1990). Early-arriving young in winter Mate protection appearsto exert its largest in- hocks were dominant to those arriving later. The fluence on female survival, and we suggestthat same situation seems to be true for other parids it is the main cause of the pattern of overlap in (see Smith 1991), including chickadees (Glase survival between the sexes. Unlike dominance 1973), and especially when there is an oppor- rank, male and female survival rates usually tunity for a young bird to pair with a widowed overlap to an extent in both chickadeesand Wil- adult (Smith 1991). It has been noted previously low Tits (Ekman 1984, Smith 1984, 1994, Hogs- 432 DAVID LEMMON ET AL, tad 1989, Ekman 1990). In chickadees,members LITERATURE CITED of the dominant pair survive the winter better AFTON,A. D., AND R. D. SAYLER.1982. Social court- than members of lower-ranked pairs (Smith ship and pair bonding of Common Goldeneyes, 1984). Ekman (1990) found a similar survival Bucephalada&a, wintering in Minnesota. Can. ranking in Willow Tits. Mate protection proba- Field-Nat. 96:295-300. bly explains this overlap in male and female sur- BROWN,J. L. 1975. The evolution of behavior. Nor- vival: benefits gained by paired females (elevat- ton, New York. CARACO,T, S. MARTINDALE,AND H. R. PULLIAM. ed feeding rate, reduced predation risk) translate 1980. Avian time budgets and distance to cover. into survival rates above those expected from Auk 97:872-875. their dominance ranks alone. Due to the influ- DESROCHERS,A., S. J. HANNON,AND K. E. NORDIN. ence of mate protection on female rank and sur- 1988. Winter survival and territory acquisitionin vival, the pattern of survival between the sexes a northern population of Black-capped Chicka- dees. Auk 105:727-736. more closely matches that predicted by a flock DICE, L. R. 1945. Measures of the amount of ecolog- structure of pairs than one of individuals. ical associationamong species. Ecology 26:297- Chickadees commonly pair for life (Smith 302. 1991), and it seems likely that mate protection DIXON,K. L. 1965. Dominance-subordinancerelation- ships in Mountain Chickadees. Condor 67:291- fosters such long-term pair bonding. For species 299. that show mate protection, this behavior proba- EKMAN,J. 1984. Density-dependentseasonal mortal- bly contributes to the enhanced reproductive ity and population fluctuations of the temperate successfound of pairs that breed together season zone Willow Tit Parus monfanus.J. Anim. Ecol. after season (see Rowley 1983). 53:119-134. EKMAN,J. 1987. Exposureand time use in Willow Tit The phenomenon of mate protection might be flocks: the cost of subordination.Anim. Behav. a general one among speciesthat remain in pairs 35:445-452. in dominance-structuredgroups during the non- EKMAN,J. 1990. Alliances in winter flocks of Willow breeding season. Benefits of mate protection Tits: effects of rank on survival and reproductive have now been documented in passerines, but successin male-female associations.Behav. Ecol. Sociobiol. 26:239-245. similar results exist for another group. In winter EKMAN,J., AND C. ASKENMO.1984. Social rank and flocks of waterfowl, females accompanied by habitat use in Willow Tit groups. Anim. Behav. their mates have a greater successin dominance 32:508-514. interactions (Scott 1980, Afton and Sayler 1982, EMLEN,S. T, AND L. W. ORING. 1977. Ecology, sexual Paulus 1983) and higher feeding rates (Scott selection, and the evolution of mating systems. Science 197:215-233. 1980, Afton and Sayler 1982) than females that FICKEN,M. S., R. W. FICKEN,AND S. R. WITKIN. 1978. are not paired. It may prove common to find that Vocal repertoire of the Black-capped Chickadee. a female’s pair-bond status in a flock during the Auk 95:34-48. nonbreeding season has a greater effect on her FICKEN,M. S., C. M. WEISE,AND J. W. POPP. 1990. fitness than her dominance rank. Dominance rank and resource access in winter flocks of Black-cappedChickadees. Wilson. Bull. 102:623-633. ACKNOWLEDGMENTS FICKEN,M. S., S. R. WITKIN, AND C. M. WEISE. 1981. K. l? Able, N. K. Bhagabati, J. L. Brown, T Caraco, Associationsamong members of a Black-capped W. G. Ellison, S-H. Li, B. Shao, S. Smith, and two Chickadee flock. Behav. Ecol. Sociobiol. 8:245- anonymousreviewers provided helpful discussionand/ 249. or comments.We are grateful to K. Beal, B. Shao, and GLASE,J. C. 1973. Ecology of social organization in J. Chen for statisticaladvice. K. P Able, J. L. Brown, the Black-cappedChickadee. Living Bird 12:235- and T Caraco kindly lent equipment. We thank R. and 267. M. Thorstenson,G. Fleweling, K. and J. Glastetter,and HAMILTON,W. D. 1971. Geometry for the selfishherd. especially R. and G. Byron for their friendly cooper- J. theor. Biol. 3 1:295-3 11. ation and generoususe of their land. We are grateful HOGSTAD,0. 1987a. It is expensive to be dominant. to E. L. Barkan for her tolerance of early mornings Auk 104:333-336. - and snowy boots. M. L. Withiam thanks E. M. Spiegel H~GSTAD.0. 1987b. Social rank in winter flocks of for help and support during the study. This research Willow Tits (Parus montanus).Ibis 129:1-9. was suuuortedbv NSF grantsBNS-8418714 to T. Car- HOGSTAD,0. 1988. Rank-related resource access in ace, [email protected] to JYL. Brown, and BSR-8313495 winter flocks of Willow Tit Parus montanus.Or- to C. l? L. Barkan. D. Lemmon and C. P L. Barkan nis Stand. 19:169-174. thank the American Ornithologists’ Union’s Van Tyne HOGSTAD,0. 1989. Subordinationin mixed-age bird Fund and the American Museum of Natural History’s flocks-a removal study. Ibis 131:128-134. Frank M. Chapman Memorial Fund for support. HOGSTAD,0. 1990. Natal dispersaland settlement of MATE PROTECTION IN CHICKADEES 433

juvenile Willow Tits Parus montanus in winter social status and resting metabolic rate in Great flocks. Fauna norv. Ser. C, Cinclus 13:49-55. Tits (Parus major) and Pied Flycatchers(Ficedula HOGSTAD,0. 1992. Mate protection in wintering Wil- hvuoleuca). Anim. Behav. 34:838-842. low Tits Parus montanus. Anim. Behav. 43:323- ROWLEY,I. 1983. Re-mating in birds, p. 331-360. In 328. F’. Bateson [ed.], Mate choice. Cambridge Univ. HOGSTAD,0. 1995. Alarm calling by Willow Tits, Press, Cambridge. Parus montunus, as mate investment. Anim. Be- SCOT, D. K. 1980. Functional aspects of the pair- hav. 49:221-225. bond in winter Bewick’s Swans (Cygnus colum- JANSSON,C. J., J. EKMAN, AND A. VON BROMSSEN. bianus bewickii). Behav. Ecol. Sociobiol. 7:323- 1981. Winter mortality and food supply in tits 327. Parus spp. Oikos 37:313-322. SMITH,S. M. 1976. Ecological aspectsof dominance JENNINGS,T., AND S. M. EVANS. 1980. Influence of the hierarchiesin Black-cappedChickadees. Auk 93: position in the flock and flock size on vigilance in 95-107. starlingsStumus vulgaris. Anim. Behav. 28:634- SMITH, S. M. 1984. Flock switching in chickadees: 635. why be a floater? Am. Nat. 123:81-98. KOIVULA,K., K. LAHTI, S. RYTK~NEN,AND M. ORELL. SMITH,S. M. 1990. Winter replacementrates of high- 1994. Do subordinatesexpose themselvesto pre- ranked chickadees vary with floater density, p. dation? Field experiments on feeding site seiec- 453-460. In J. Blondel, A. Gosler, J.-D. Lebreton, tion bv Willow Tits. J. Avian Biol. 25:178-183. and R. McCleery reds.], Population of passerine birds, an integrated approach. Springer-Verlag, KOIVULA,i<., AND M. ORELL. 1988. Social rank and Heidelberg. winter survival in the Willow Tit Parus montanus. SMITH, S. M. 1991, The Black-capped Chickadee. Omis Fennica 65:114-120. Comstock Publishing, Ithaca, NY. LENDREM.D. W. 1983. Predationrisk and vigilance in SMITH,S. M. 1994. Social influenceson the dynamics the Blue Tit Parus caeruleus. Behav. Ecol. Socio- of a northeasternBlack-capped Chickadee popu- biol. 14:9-13. lation. Ecology 75:2043-205 1. MILTON, J. S., AND J. V. TSOKOS.1983. Statistical WEISE,C. M. 19%. Sex identification in Black-cap- methodsin the biological and health sciences.Mc- ued Chickadees.Milwaukee Fld. Sta. Bull. 12:16- Graw Hill, New York. is. ORR, G. D., AND A. M. VERBEEK.1981. Female de- WI~ENBERGER,J. E 1979. The evolution of mating mands: some fitness implications in chickadee systemsin birds and mammals, p. 271-349. In P. flocks. Can. J. Zool. 62:2550-2552. Marler and J. Vandenbergh teds.], Handbook of PAULUS,L. 1983. Dominance relations, resourceuse, behavioral neurobiology. Plenum Press, New and pairing chronology of Gadwalls in winter. York. Auk 100:947-952. WITTENBERGER,J. E, AND R. L. TILSON. 1980. The R~SKAFT,E., M. JARVI,M. BAKKEN,C. BECH,AND R. evolution of monogamy: hypotheses and evi- E. REINERTSEN.1986. The relationship between dence. Annu. Rev. Ecol. Syst. 11:197-232.