Mobbing by Florida Scrub Jays: Behaviour, Sexual Asymmetry, Role of Helpers and Ontogeny

Anirn. Behav., 1989, 38, 795-816

Mobbing by Florida scrub jays: behaviour, sexual asymmetry, role of helpers and ontogeny

ANN MARIE FRANCIS*t, JACK P. HAILMANI" & GLEN E. WOOLFENDEN:~ t Department of Zoology, University of Wisconsin, Madison, Wisconsin 53706, U.S.A. Department of Biology, University of South Florida, Tampa, Florida 33620, U.S.A.

Abstract. Behavioural patterns used in mobbing predators by the cooperatively breeding Florida scrub jay, Aphelocoma c. coerulescens, are described from films, field observations and field experiments. The roles of individual group members and the ontogeny of mobbing by fledglings were investigated experimentally by releasing a 1.6-m snake in the presence of jays. Jays used at least nine action patterns and one variable vocalization in mobbing. Male breeders mobbed most intensely, female breeders and helpers mobbed with lesser and approximately equal intensity, and fledglings mobbed the least. Fledglings began mobbing by 47 days post-hatch and gradually acquired adult-like mobbing behaviour by 3 months of age. Coordinated flying ability may be necessary before fledglings begin to mob. Mobbing fledglings were often ignored by adults that had not yet seen the predator. A comparison of the mobbing of the Florida scrub jay with other congeners indicates that several aspects of mobbing behaviour may be related to the social system of the birds.

Avian mobbing consists of behaviour in which The Florida scrub jay has a social system in birds gather around a predator and vocalize loudly which the monogamous breeding pair and its or perform conspicuous visual displays. Many 'helpers' occupy permanent territories of at least explanations have been proposed for mobbing several hectares. Yearling, and often older, jays (Curio 1978); all include the idea that mobbing is remain in their natal territories and function as somehow anti-predator in nature (but see Slags- non-breeding helpers (although helpers are occa- void 1984). Avian mobbing is usually social, with sionally adopted non-offspring of the pair helped). members of the social group and often other The helpers participate in defence of the territory conspecifics and even heterospecifics being and nest, sentinel duty during foraging, mobbing of attracted to the site (e.g. Hinde 1952; Altmann predators, feeding of nestlings and fledglings, and 1956; Cully & Ligon 1976), removal of faecal sacs; but they do not participate New World jays of the genus Aphelocoma exhibit in nest building, incubation or brooding. Breeding strong mobbing responses that are similar among pairs with helpers produce more offspring than species, but with differences that seem to be related those without (Woolfenden 1973, 1975; Woolfen- to differences in social systems. The mobbing den & Fitzpatrick 1978, 1984), and the specific behaviour of the grey-breasted (formerly 'Mexi- mechanisms of increased breeding success are can') jay in New Mexico and Arizona, A. ultramar- currently under intensive investigation. Breeders ina arizonae, and the western scrub jay in New with helpers also have a higher rate of survival, Mexico and Texas, A. coerulescens woodhouseii, perhaps because of increased efficiency of the has been compared by Cully & Ligon (1976). Grey- predator alarm system in larger family groups breasted jays live year-round in communal flocks in (Stallcup & Woolfenden 1978; Woolfenden & which some group care of nestlings and fledglings Fitzpatrick 1984). Food provided by helpers con- exists, whereas western scrub jays occur in pairs tributes httle to increase survivorship of young. that defend territories from one another all year Much of the mortality is thought to be caused by (Gross 1949; Hardy 1961; Brown 1963, 1970, 1972, predation: 90% of nesting failures and virtually all 1974). In this study, the mobbing of snakes by fledgling loss are probably caused by this factor, Florida scrub jays, A. c. coerulescens, a congener but the causes of adult mortality are less certain. with still another social system, was investigated. Certain snakes, mammals and birds are able to prey * Present address: 7081 NW 16th St., Apt. 105B, Plan- on both scrub jay nestlings and fledglings (Westcott tation, FL 33313, U.S.A. 1970; Woolfenden 1978; Webber 1980; Woolfen-

0003-3472/89/110795+22 $03.00/0 1989 The Association for the Study of Animal Behaviour 795 796 Animal Behaviour, 38, 5

{a) Snake bag

Stri:gooden

0 ~ring ~ Treetrunk

Top view Side view

(c ( b ) (f~- Snake

!iiiiii!iiiiii!ii ii! Woo e ,ro e Spool of / monofilamentline

collar

Stnng

Figure 1. Experimental apparatus: (a) before the beginning of a trial, (b) bag being removed from around snake, (c) snake collar and spool of monofilament line. See text for details. den & Fitzpatrick 1984; Mumme 1987). Defence This study describes the responses of Florida against predation is thus an important potential scrub jays to predatory snakes and compares the role of helpers. Woolfenden suggested (1978, pp. responses of the different group members. Jays kill 15-16) that 'the major way that Florida scrub jay and eat small snakes (less than about 30 cm), ignore helpers help is by decreasing predation on the nest those of intermediate size, and readily mob those containing eggs or nestlings, and to some extent on larger than about 60 cm (Amadon 1944; Woolfen- the scattered fledglings, of the breeders with which den & Fitzpatrick 1984). In particular, special they affiliate'. emphasis was placed on differences in mobbing Francis et al.: Florida scrub jay mobbing 797 between male and female breeders, between helpers season and showed no adverse effects as a result of and breeders, and between fledglings of different the trials. Treatment of the snake conformed to all ages. current animal care guidelines.

METHODS Experimental Procedure Study Population and Site Only scrub jay groups with nestlings or fledglings were used. If the young of a given pair The study was carried out from April to August disappeared over the course of the summer, their 1981 at Archbold Biological Station, Highlands social group was not tested again. Each of 20 County, Florida. A marked population of Florida groups was exposed to the snake a maximum of scrub jays has been under study by G. E. W. and his three times from 31 May to 9 August, between the co-workers since 1969 (see Woolfenden & Fitzpa- hours of 0700 and 1030 hours Eastern Daylight trick 1984). In a study tract of about 400 ha, Time. Within each set of trials the order in which virtually all jays are individually colour-banded, groups were tested was determined randomly. A and the sexes, ages, relationships and territories of given group was not tested until at least 1 week had most of the jays are known. Many of these birds elapsed since the previous trial with that group. have been habituated to human observers (Wool- An experimental trial was begun when all jays in fenden 1973, 1975). the group were present. During the initial 50-days The scrub jay habitat consists of open oak scrub post-hatch period, when the young jays were in growing on old sand dunes. The dominant peren- nests or were fledged but relatively immobile, the nial vegetation consists of scrubby (1-2 m) oaks, snake bag was placed approximately 4 m from the Quercus spp., palmettos, Sabal etonia and Serenoa young. Later, when the fledglings began to move repens, and scattered pine trees, Pinus elliottii and about more freely, a set distance was impossible to P. clausa. Sandy areas containing grasses, herbs or maintain and the snake was released wherever the no vegetation are prevalent (see photographs in jays were found within their territory. The snake Woolfenden & Fitzpatrick 1984). was placed in a different location for each trial to prevent the jays from associating a particular site Apparatus with the experimental procedure. Mobbing was studied experimentally by releas- The snake was released and observed from a ing a live snake in the presence of a scrub jay group. distance of 3 m, with running notes being taken on The snake was a male Florida pine snake, Pituophis a cassette tape-recorder. General behaviour of the melanoleucus mugitus, that had been in captivity for snake, such as moving, coiling, facing birds and 3 years. The snake was 1.6 m long, weighed about flicking the tongue, was recorded. For each scrub 955 g, and was large enough to eat an adult jay. jay, data consisted of the horizontal distance from Pine snakes occur within the study tract and are the snake, height above the ground (vertical dis- mobbed by the jays; pine snakes are constricting tance), occurrence and type of vocalizations, colubrine snakes that eat primarily small mammals general behaviour of a non-mobbingjay (such as and birds (Conant 1975; Smith & Brodie 1982). preening, foraging, etc.), and specific action pat- The pine snake was released from a cloth bag terns of a jay that was mobbing or was otherwise placed on the ground at the edge of an open sandy reacting to the snake or to other mobbers. Horizon- area. The bag was positioned to face the open area tal and vertical distances were estimated by eye and so that the snake would initiallybe visible to nearby were occasionally checked with a tape. A trial jays. The snake bag could be opened from a terminated either after all group members flew distance of 3 m by pulling a string (Fig. la). If the farther than 15 m from the snake or until at least snake did not leave the bag spontaneously it was 1 rain had elapsed since any jay had last responded forced out by drawing the bag through a rectangu- to the snake. After each trial the duration of each lar wooden frame (Fig. la, b). The snake was behavioural pattern was timed with a stopwatch tethered to a spool of monofilament line (Fig. lc) from the tape recording. Straight-line distances by means of a Velcro collar fastened snugly between jays and the snake were calculated from between the head and the enlargement of the body the vertical and horizontal distances by means of at the heart. The snake was healthy at the end of the solving right triangles. 798 Animal Behaviour, 38, 5

In some trials (especially those involving large A scrub jay 'detected' the snake's presence when groups) only the adults or fledglings could be the jay responded in a visible or audible manner: followed. In these cases a coin was flipped to fixing the binocular gaze in the snake's direction, determine which age class would be observed. If the approaching the snake, hopping or flying away entire social group could not be watched in the from the snake and then looking at it, or giving a following trial, whichever class within the group mobbing call. A jay 'discovered' the snake if it was that had not been observed previously was the first jay in the group to detect it. In some cases, observed in the next trial. more than one jay seemed to discover the snake To compare mobbing with responses to a novel simultaneously. The latency between detection and or suddenly appearing object and to ensure that the start of mobbing is the time at which a jay began jays would not learn to associate the experimental mobbing minus the time at which this jay detected apparatus or the observer with the snake, control the snake. trials were carried out. In these control situations The percentage of time spent mobbing is the the empty snake bag was positioned and opened as total time spent mobbing divided by the time described above and the jays' behaviour was noted. available for mobbing, the fraction multiplied by Three controls were run with each group before the 100. The time available to a jay is the time the last first experimental trial, one for each group between mobber in the jay group stops mobbing minus the the first and second trials, and one for each group time at which the focal jay detects the snake. If between the second and third trials. during this period the jay spends some time defending the group's territory against conspecific intruders, the time spent in defence was subtracted Determination of Action Patterns from the time available. Per cent-time-mobbed Nine action patterns used by mobbing scrub jays rather than the absolute mobbing time is used to were described from field notes by A. M. F. of compare group members because the jays detected natural and experimental mobbing situations, and the snake at different times and because some from slides by A. M. F. and J. P. H. and 16-mm departed to defend the territory while others did movie films (at 24 frames/s) by J. P. H. Body not. During several trials at least one group postures and angles were estimated in the field and member departed after the start of the trial but were measured with a protractor from the slides before the snake was detected by any other jays. and movies, and several action patterns were timed Jays that departed in this way often returned after by counting frames in the films. Mobbing calls were mobbing began and then also began to mob. If the recorded with a Uher Report-L recorder running at mobbing response waned over time (see Hinde 19 cm/s and a Uher M516 dynamic microphone. 1954), these late-arrivingjays sometimes continued Sound spectrographs of these calls were made on a to mob after the first mobbers in the group had Kay 6061B Sonagraph using a wide band (300 Hz) already stopped responding to the snake. Because setting and either a 0.08-8.0 kHz or a 0.16-16.0 the time available for mobbing is currently defined kHz frequency range. to end at the time when the last group member stops mobbing, this variable is biased in favour of late arrivals. To eliminate the bias in trials where Definitions jays arrived late, the time available for the jays Classes of scrub jays were: male and female present from the beginning was modified in the breeder, male and female helper (adult non- following way. In three of 52 trials (5.8%) the jays breeders), and fledgling (young of the year). We present throughout the trial did not mob at all after define mobbing as behaviour directed toward a newly arrived jays began to mob. In these trials the potential predator of eggs, young or adults in time available to the original mobbers ended when which a scrub jay gives a specific mobbing call, the last of the original mobbers stopped mobbing. binocularly fixates the predator from a distance of In five trials (9.6%) the jays present from the start 10 or fewer body-lengths (about 3 m) while in full of the trial recommenced mobbing after late- view of the predator, or performs one of the other arriving jays began to mob. In these cases, the time eight action patterns described in the Results. Jays between the start of this new mobbing bout and the within 3 m were very likely to mob more actively end of the previous mobbing episode was sub- within a few seconds, whereas birds farther away tracted from the time available to the original were likely to continue merely to watch quietly. mobbers. Francis et al.: Florida scrub jay mobbing 799

The 'closest approach' is the shortest total number of jays in the group). For each group the distance seen between a mobbing jay and any part probability of any jay of a given class being the last of the snake's body. 'Responding to mobbers' is mobber was the number of jays in that class in the behaviour exhibited by fledglings in which they group (N) multiplied by the reciprocal of the group react to the mobbing of other group members size (N/n). The overall expected value for jays in a rather than mobbing themselves. The responses certain class being last mobbers was the sum of the include watching the adults mob, moving about probabilities associated with this category in all the rapidly in an agitated manner, or reacting to groups mobbing calls as though a message conveyed by the g call is one of warning. The 'percentage of time spent ( ~ Ni/n~, where g is the number of groups). i=1 responding to mobbers' is the time spent respond- In all tests, jays present were used to compare per ing divided by the time available, the fraction cent-time-mobbed, time mobbed, per cent-time- multiplied by 100. The time available is defined as responded-to-mobbers, and discovery of the snake. the per cent-time-mobbed (above) minus the time However, for latency, closest approach, last mob- during which no mobbers existed to which a ber and per cent-time-responded/per cent-time- fledgling could respond. An index employed for mobbed only jays that actually mobbed were fledgling behavior is the per cent-time-responded- included. This is because a latency period, closest to-mobbers divided by the per cent-time-mobbed, approach, and last mobber by definition do not as long as the denominator is not equal to zero. exist for non-mobbers, and the denominator of per cent-time-responded/per cent-time-mobbed would Statistical Tests equal zero in a non-mobber. Standard non-parametric tests (Siegel 195~ Rohlf& Soka11969) were used throughout, as citec RESULTS in Results. In comparisons of individuals with themselves in trials 1 and 2, all jays present in both Action Patterns of Mobbing Observed of these trials were included. To compare trials 2 In both natural and experimental mobbing, and 3 or trials 1 and 3, however, only jays that scrub jays used several distinct action patterns (Fig. detected the snake in all three trials were used so 2). Barbour (1977) termed the mobbing vocaliza- that all the jays had equal experience of the tion (N> 141 heard) the 'predator screech scold'. experimental situation. The call is a harsh vocalization given while on a In the correlations involving fledgling age, each perch, on the ground or in flight. Calls covered a trial was analysed separately as well as all three wide frequency range, approximately 1-8 kHz, and together. Because experience in mobbing is likely to lasted about 0.3 s; they were sometimes given singly be important in the ontogeny of this behaviour, the but more commonly in a long series. Calls varied correlations for the first trial include all the trials in somewhat in acoustical structure but no attempt which a fledgling was first exposed to mobbing of was made to record and analyse this variation. the pine snake. The first trial for a fledgling may be The only other vocalization directed toward a the second or third trial for the group if the predator in this study was that termed 'snarl' by fledgling was not present when the other jays Barbour (1977), delivered by a male breeder in mobbed, or if no mobbing occurred in a trial. response to a wild 120-cm-long eastern indigo Similarly, the second and third trials include only snake, Drymarchon corais couperi. The jay was fledglings that were present for exactly one and two perched 150 cm above the ground, next to his nest, previous trials in which mobbing took place, containing 6-day-old nestlings, when he saw the respectively. snake on the ground about 180 cm from the nest In order to compare jays in different classes with shrub. The jay gave a short, harsh snarl while flying respect to which stopped mobbing last, the data toward the snake. The snake began to move away were compared with expected values. To calculate from the nest rapidly and the jay followed it on the the expected values, all jays were considered to ground until it disappeared from sight in the have equal probability of being a last mobber. In vegetation. each group, this probability for each jay was the While on a perch or the ground, jays binocularly reciprocal (l/n) of the group size (where n is the fixated the snake silently and motionlessly (N> 63 800 Animal Behaviour, 38, 5

8 ~'la) N ~e

g444 4 D" ~2 .... /b) (c) i Jlllll q T ....ILIL 0.4 0.6 0.8i 1.0 1,2 0.2 Time ( s )

(e) (fl

Figure 2. Action patterns of mobbing: (a) sonagram of mobbing calls, (b) binocular fixation, (c) orient toward, (d) flick tail, (e) extend upward, (0 jump, (g) bob, (h) peck perch, (i) flick wings and (j) bite snake.

observed). The duration varied from a few seconds held at most for a few seconds. While the jay was up to about 1 min. Orientation toward the predator perched or on the ground, and in a variety of body (N:=41 recorded) may occur on the ground, level positions, the tail was raised suddenly to 30-90 ~ with the predator, but much more commonly the above the long axis of the body ('tail-flick', N= 67 jay was perched above the predator. The tail, body- observed). The tail was sometimes spread momen- axis, head and bill were in a line that pointed tarily just prior to being raised. This movement toward the mobbed animal. This posture may be occurred singly or as a series of flicks and was Francis et al.: Florida scrub jay mobbing 801 usually accompanied by a mobbing call. A tail-flick upward so that the tips were raised above the back. was included in a bob (below) and occurred with This upward component varied in amplitude from wing-flicks (below) or alone. A lone tail-flick takes a slight raising to an almost vertical posture of the about 0.25 s (measured from the films). wings. (3) The primaries were spread. This compo- The 'extend upward' (N=29 observed) was nent occurred during the upward rotation, and behaviour in which the jay extended its legs until only during high-amplitude wing-flicks. If wing- the angle of the tarsal joint was 140-150 ~ and tilted flicking occurred with tail-flicking, the wings were the body upward so that the breast was 70-80 ~ raised slightly before the tail. Wing-flicks take above horizontal. The neck was stretched vertically about 0.125 s (measured from the films) or less. and the head, neck, back and breast feathers were The biting of a snake (N= 12 observed) consisted sleeked, This posture was held for at least a few of five steps. (1) The jay slowly approached, by seconds, often while hopping slowly toward the hopping from behind the tail of a snake that is predator. Jays used their legs and wings to jump moving away from the bird. The breast and back (N=20 observed) into the air. The bird landed feathers were sleeked. (2) The jay stopped, leaned immediately with wings and tail spread and the tail forward by flexing the hip and tarsal joints, and held high. A jay landed where it started or up to 30 stretched the neck forward. (3) The jay opened the cm away; it did not necessarily land facing the bill and then closed it on the snake's tail, usually predator. If the jay changed its orientation during within 5 cm of the tip. (4) The jay sometimes pulled this jump, the change was accomplished in mid-air. its head back and leaned backward before releasing A 'bob' (N=30 observed) occurred on the the tail, thus pulling it. (5) The jay released the tail ground but was more common while the bird was and jumped as described above, usually landing perched. Five distinct steps constituted a single 15-30 cm behind the snake. Occasionally, a scrub bob. (1) The bird perched with wings folded, with jay would bite the snake twice in rapid succession. the head, body and tail in a straight line in which In all cases the snake moved forward rapidly for the head was above the tail, and with an angle of about 15 cm immediately after being bitten. A about 120 ~ at the tarsal joint. (2) The legs were snake was never seen to turn and threaten a bird flexed, reducing the angle to 60 ~ and bringing the that had just bitten it. body closer to the toes. (3) The neck was retracted, Flicking the tail and wings, extending upward, which pulls the head closer to the shoulders, and jumping and bobbing were seen in contexts other the jay inclined forward at the hips until the body than mobbing, such as in territorial defence and was horizontal or the anterior was as much as 30 ~ pre-flight behaviour (as evidenced by field observa- below horizontal. The tail was held motionless tions and films of non-mobbing scrub jays). Conse- while the body moved. (4) The tail was flicked quently, these action patterns are probably derived upward suddenly (see above) and the head was from incipient movements of flight (so-called raised more slowly. (5) The bird returned to the flight-intention movements; Daanje 1951). The five starting position by first raising the body, and then remaining action patterns were not seen in other lowering the tail. Sometimes the tail was spread contexts and therefore do not seem to be related to while it was lowered. Bobs occurred singly or in flight. series. Each bob took about 0.21 s (measured from the films) and was often accompanied by a mobbing call or by wing flicks (see below). Field Observations of Mobbing The 'peck perch' (N= 17 observed) occurred with bill closed or nearly closed and wings folded; Scrub jays have been observed intensively at the the neck arched to point the bill vertically down- Archbold Biological Station since 1969. The ward while the legs were slightly extended. The legs reports of observers with long experience watching then flexed, the body inclined forward and the tail the jays (e.g.A. Margaret Elowson, John W. lowered as the jay pecked the perch between its feet. Fitzpatrick, Kevin J. McGowan, Ronald L. At least three motor components composed a wing- Mumme and the authors) agree and produce the flick (N= 23 observed). (1) The wings were rotated following general picture of mobbing. To date, the outward and upward at the shoulder joint so that list of species known to be mobbed includes 10 the plane of the wings was horizontal at the level of reptiles (of which nine are snakes), two birds and the jay's back. (2) The wings were then flicked eight mammals (Table I). The opinion of all 802 Animal Behaviour, 38, 5

Table I. Animals reported to be mobbed at least occasionally by Florida scrub jays*

Common name Scientific name Authority

Racer Coluber constrictor Barbour 1977, J. P. H,, G. E. W. Coachwhip Masticophis flagellum Barbour 1977, Webber 1980, Lohrer 1980, J. N. Layne, A. M. F., G. E. W. Indigo snake Drymarchon corais Barbour 1977, J. N. Layne, A. M. F., G. E. W. Corn snake Elaphe guttata Barbour 1977, A. M. F., G. E. W. Rat snake Elaphe obsoleta A. M. F., G. E. W. Pine snake (bullsnake) Pituophusmelanoleucus A. M. Elowson, G. E. W. Eastern coral snake Mierurusfulvius J. N. Layne, A. M. F., G. E. W. Pigmy rattlesnake Sistrurus miliarius J. N. Layne Eastern diamondback Crotalusadamanteus Barbour 1977, G. E. W. rattlesnake American alligator Alligator mississippiensis K. J. McGowan Great horned owl Bubo virginianus Barbour 1977, A. M. Elowson, G. E. W. Eastern screech-owl Otus asio G. E. W. Nine-banded armadillo Dasypus novemcinetus Barbour 1977 Grey fox Uroeyon, cinereoargenteus G. E. W. Domestic dog Canis lupus A. M. F., G. E. W. Racoon Proeyon lotor Barbour 1977, G. E. W, Longtail weasel Mustelafrenata G. E. W. Bobcat Lynx ruJus A. M. Elowson, A. M. F., J. P. H., G. E. W. House cat Felis eatus G, E. W. Man Homo sapiens J. P. H., G. E. W.

* Observations by authors of this study indicated by initials; other unpublished observations are personal communications.

experienced observers is that mobbing is elicited by Many species of large vertebrates encountered snakes larger than 60 cm. by the jays are not mobbed: gopher tortoises, The snakes mobbed most often are coachwhips, Gopherus polyphemus; eastern cottontail rabbits, Masticophisflagellum, and indigo snakes, both of Sylvilagus floridanus; white-tailed deer, Odocoileus which regularly exceed 2 m in length. Jay observers, virginianus; and domestic cattle. Armadillos are and no doubt the jays themselves, see more racers, abundant in the scrub and are seen frequently by Coluber constrictor, than any other snake; how- the jays. The one literature report of jays mobbing ever, few of these are mobbed by the jays, probably an armadillo (Barbour 1977) might have occurred because of their great speed. The pine snake (the because the mammal was present during mobbing species used in experiments below) are seldom seen, of a snake that had disappeared from view. Several but probably rank third or fourth among snakes in species of herons and sandhitl cranes, Grus cana- frequency of being mobbed. Observers have densis, occur irregularly in the study tract, and are encountered only three eastern diamondback not mobbed. rattlesnakes, Crotalus adamanteus; G. E. W. was Several primarily nocturnal predatory mammals led to two by mobbing jays. The mobbing of coral that live in the scrub are rarely encountered by the snakes, Micrurusfulvius poses a question. At least diurnal jays. Examples include the racoon, opos- two of the four or five coral snakes that had been sum, Didelphis marsupialis, and spotted skunk, mobbed fell within the size range of snakes that jays Spilogale putorius. Domestic dogs and house cats ignore, and were close to the size range of those are rare in the study tract. On the rare encounters, eaten by the jays (smaller species such as Thamno- however, jays do mob some of these mammals phis sauritus, Opheodrys aestivus, Diadophis puncta- (Table I). tus, possibly Cemophora eoccinea). Are coral After snakes, jays probably most often mob snakes mobbed because their venom poses a danger bobcats and great horned owls, nocturnal preda- to scrub jays? tors occasionally encountered during the day. We Francis et al.: Florida scrub jay mobbing 803 have no records of jays mobbing diurnal raptors. both times the birds escaped. The male breeder When suddenly confronted with a sharp-shinned faced off with the coiled snake and delivered several hawk, Accipteir striatus, Cooper's hawk, A. coo- pecks to the snake's head. perii, northern harrier, Circus cyaneus, or merlin, G. E. W. has also made a few observations of Falco columbarius, the jays give an alarm call and jays killing small snakes upon which they feed. In dive for cover. Other raptor species, or the four just these cases the jays jab just at the base of the snake's named if sighted at a distance, are simply watched. skull. Perhaps this behaviour explains why snakes To date, we have evidence of predation on the hide their heads beneath body coils when being marked jays by the coachwhip, indigo snake, severely mobbed by jays. Cooper's hawk, northern harrier, great horned owl, Bubo virginianus, and screech-owl, Otus asio, bobcat, domestic cat, Fells catus, and probably Mobbing Experiments merlin. We have seen near misses by sharp-shinned The 52 experimental mobbing trials involved 20 hawks. different scrub jay groups. In two trials, the groups On 7 April 1974 G. E. W. watched a scrub jay had only nestlings, in 48 they had only fledglings, perched in a citrus tree about 1 m above a coiled and in two trials the groups had both fledglings and pine snake. The jay hopped down to less than 0.5 m nestlings from different broods. (The existence of from the snake and dropped a twig on it. The twig true second broods is rare in the Florida scrub jay.) missed and the snake remained coiled. Later, The mean time spent mobbing the pine snake was G. E. W. flushed the snake, and as it crawled off 187-4 s, (range 0-784 s). This mobbing time through open grass another member of the jay corresponds to a mean per cent-time-mobbed of group pecked its tail. Dropping objects on snakes 46.2% (range 0-100%). No clear relationship exists was not seen during experiments reported below; between the time available and the time spent the act may function to make snakes move, so the mobbing (Fig. 3). The mean latency between seeing jays can mob and chase. the snake and commencement of mobbing was 35.0 Of mobbed snakes watched by A. M. F. (Table s (range 0-588 s) and the mean closest approach of I), all except the coachwhip either began to move or mobbing jays to the snake was 155.3 cm (range 0- to move noticeably faster soon after mobbing 915 cm). began. The rat snake, Elaphe obsoleta, moved In the control trials, jays responded to but did slowly, the others rapidly, and the jays landed on not mob the experimental apparatus in five cases the ground close to the snake. In contrast, while out of 94. (Jays mobbed in all experimental trials.) mobbing the bobcat and dog (A. M. F. observa- In four control trials one or two group members bit tions in Table I), the jays remained on top of the the bag, and in the fifth a single jay approached to low oak shrubs while giving mobbing calls. The look at the bag. Three of the five responses bobcat appeared to ignore the mobbing jays and occurred in control trials before any actual mob- the dog sniffed around the base of the shrub and bing trial with the snake had been conducted. Jays watched the jays before moving off. J. P. H. react similarly to other novel objects such as observed and photographed jays mobbing a bobcat canteens, boot laces and tape-recorders; we inter- in a different episode, and these jays remained on pret the jays' responses to the bag as investigative top of a fence 1.5 m high. behaviour. G. E. W., with help from Ralph W. Schreiber, In most cases, a mobbing assemblage consisted conducted observations on mobbing using a teth- of all the members of the jay group in whose ered racer about 1 m long. On 23 April 1970, the territory the snake was placed. Fledglings from snake was released on the ground beneath a nest neighbouring groups also participated in 11 trials. with nestlings. The tether entangled in the shrubs Fledglings often wander through territories other and all five jays in the group pecked the snake in than that of their parents, and are usually tolerated several places, especially on the vibrating tail. The temporarily (Woolfenden & Fitzpatrick 1977). In confined snake seemed to hide its head beneath its only one case did a pair of neighbouring adults body coils. The tether was then attached on the cross territorial boundaries to approach the snake. snake's tail, again it entangled in the shrubbery, Birds of other species were often attracted by and again all five jays attacked. The snake coiled mobbing scrub jays: northern flickers, Colaptes and struck several times, striking jays twice, but auratus; red-bellied woodpeckers, Melanerpes car- 804 Animal Behaviour, 38, 5

I000 / / / / / /

800 - / e / /o / / / / 600 -- Q / / | E /o / A g / 400, -- _/__ /0 o O E

OOA O~

_ Q O/~176 ~ ~ ~ _ AO 200 ,ej~ ~ A. _ . 10 A

'l,r~ ,~ '~ . ~ ~_,+ I 0 200 400 600 800 I000 1200 Time available (s) Figure 3. Time spent mobbing versus time available for all three trials. The dashed line indicates where time spent mobbing equals time available, o: adults; zx: fledglings. olinus; blue jays, Cyanocitta cr&tata; northern mean difference between the times that the first and mockingbirds, Mimus polyglottos; brown last family members stopped mobbing was 92.2 s if thrashers, Toxostoma rufum; loggerhead shrikes, the snake disappeared and 140.9 s if the snake Lanius ludovicianus; and rufous-sided towhees, remained visible; the difference was statistically Pipilo erythrophthalmus (male and female adults significant (Mann-Whitney U-Test, P = 0.0495, and fledglings). Of these, only towhees joined the two-tailed). When the pine snake remained fully or scrub jays in calling persistently and in approach- partially visible, some jays continued to mob for ing to within a few metres of the snake. several minutes after other group members had Mobbing sequences were often punctuated by stopped. periods of activity that seemed unrelated to the For jays that had more than one mobbing predator. Most of the jays (92.0%) spent some time episode in a trial, the lengths of each jay's mobbing foraging, preening, defending the territory, looking episodes were compared (Wilcoxon test). Mobbing about the territory from a high perch (presumably episodes were included only if they did not end sentinel behaviour), feeding young (only adults), or prematurely because of the disappearance of the begging (only fledglings). Occasionally (2.6% of all snake or the appearance of territorial intruders. In observations), such behaviour was performed trial 1 and in all trials combined, the second within 1 m of the snake. mobbing episode was significantly shorter than the first (Table II), but in trials 2 and 3 no differences existed. Furthermore, no significant differences Snake Movement and Jay Response occurred between the lengths of the second and If the snake crawled into vegetation so that it third or the third and fourth mobbing episodes. could not be seen (seven trials out of 52), the These data suggest that the predator provides a cessation of mobbing was more synchronous than mobbing stimulus as long as it is visible, but that if the snake remained visible. When the snake the effectiveness of the stimulus decreases with passed out of view, all jays stopped mobbing within time. 1 min except for a male helper on one occasion. The The most common behaviour of the snake in the Francis et al.: Florida scrub jay mobbing 805

Table II. Means, standard errors and statistical comparisons of mobbing episode durations within trials (s of continuous mobbing)

One-tailed N )? sE P (WilcoxonTest)

Trial 1 First episode 24 178.7 2%6 Second episode 24 73.2 15,4 < 0.0048 Trial 2 First episode 19 96.3 19.4 Second episode 19 69.5 12.1 NS Trial 3 First episode 16 125.2 29.8 Second episode 16 72.4 14,0 NS All trials combined First episode 59 137.6 16.2 < 0.0005 Second episode 59 71.8 8.1 Third episode 20 86-8 16.1 NS Fourth episode 8 47.9 12.2 NS

presence of mobbingjays was to remain motionless viour, in which a male breeder appeared to check (31 of 52 trials), except for occasional tongue flicks. on his fledglings while mobbing a coachwhip; the However, in almost half of the trials (21) the snake call results in cessation of the young's begging. began moving after the onset of mobbing, and in 14 '~ In five of 11 trials (45.5%) in which a fledgling of these he moved into vegetation or under dead was the first group member to detect and mob the leaves where he was at least partially hidden. When snake, the adults seemed to ignore the fledgling's the snake did move, he travelled an average behaviour. In two of these cases the fledgling did distance of 309.4 cm. No correlation existed not vocalize and this young bird was the only between the distance moved and the number of mobber until an adult noticed the snake more than mobbers (Spearman's rs=-0"23, one-tailed 3 rain later. In the three trials where the discoverer P>0.05). Several times movement by the snake did give mobbing calls, the other fledglings in the caused renewed or intensified mobbing. Less com- group immediately joined in mobbing. However, mon responses to mobbers were for the snake to the nearby adults did not appear to search for a pull his head closer to his body (N= 3), place his predator. In these three cases, an adult saw the head under a coil of his body (N= 2), or turn his snake more than 4 min after the fledglings had head toward a mobbing jay, causing it to jump begun to call and this new 'discoverer' then began back (N= 5). to mob. In the one case where a second adult was still nearby, this jay immediately responded to the Adult-Fledgling Interactions adult mobber's calls by approaching the snake. Unlike fledglings, mobbing adults were never During the experimental trials, four jays (a male ignored. When an adult began to mob, the other helper, a male breeder and two female breeders) jays looked where the mobber was looking, usually temporarily stopped mobbing and appeared to within a few seconds. If jays were out of sight when check the nestlings or young fledglings, or warn an adult gave a mobbing call, they often returned to them of danger. The male breeder gave a 'single the group immediately. sharp weep' (Barbour 1977) when one of the fledglings flew a few metres above the snake, and Mobbing Behaviour by Fledgfings of Various Ages one female breeder gave this call while flying to her fledgling. Webber (1980) reported similar beha- All of the fledglings involved in the mobbing 806 Animal Behaviour, 38, 5 trials were at least 47 days post-hatch and able to trials are combined (rs= 0.38 for trial 1, -0"29 for fly well. Younger fledglings, from day of fledging trial 2, 0.20 for trial 3, P>0-05 for all; r,.= -0-42 (around 17 days) to 33 days post-hatch were and P < 0.0005 for all trials combined). Dividing observed on seven occasions when adult jays gave the per cent-time-responded by the per cent-time- mobbing calls or 'single sharp weeps' (Barbour mobbed gives an indication of how these two 1977) to predators or humans. In these seven cases variables changed relative to each other. A negative begging fledglings became silent and all fledglings correlation exists between this index and age in became motionless. Two broods (23 and 33 days combined trials (rs= -0'08 for trial 1, -0.30 for old) scurried under vegetation as soon as an adult trial 2, 0.20 for trial 3, P> O.lO for each; rs= -0"38 called, where they remained motionless for 5 and 7 and P < 0'005 for combined trials). min, respectively. The 23-day-old fledglings remained hidden and silent for an additional 14 First and Last Mobbers min, occasionally stretching their legs and wings. In the mobbing experiments the age of the With a single exception, the jay that discovered fledglings ranged from 47 to 101 days in the first the snake began the mobbing. Therefore, no scrub trial, 70 to 116 days in the second, and 98 to 126 jay class consistently began mobbing bouts unless days in the third. The percentage of fledglings that one consistently discovered the snake. Male mobbed the snake increased from 79.4% in trial 1 breeders were the discoverers (or co-discoverers) in to 88.0% in trial 2 and 86.7% in trial 3. Although 42.9% of the trials, female breeders in 15-8%, male the per cent-time-mobbed increased after trial 1, no helpers in 25"0%, female helpers in 6.2% and correlation exists between this variable and fled- fledglings in 25-7%. Comparisons of different jays gling age (Spearman's rs=0"07 for trial 1, 0.09 for within the same group (male breeder versus his trial 2, 0.34 for trial 3, -0"01 for all trials mate, male breeder versus helpers, etc. for a total of combined, P>0.05 in all cases). The latency six such comparisons) reveal a single significant between detection and mobbing was shorter for difference in discovery of the snake: male breeders older fledglings, with a significant negative correla- discovered the snake more often than female tion when the trials are combined (r,= -0.26 for breeders when the three trials are combined (sign trial 1, 0.15 for trial 2, -0-44 for trial 3, P>0.10 in test, two-tailed P=0.008). The observed and all three cases; rs=--0.36 for combined trials, expected values of group members that were the P< 0.025). Closest approach also decreased with last to stop mobbing are shown in Table III. The fledgling age. All correlations between closest trend was for male and female breeders to be the approach and age are significant except in the first last mobber more often and for helpers and trial (r~= -0'10 and P>0.10 for trial 1; rs= -0.74 fledglings to be the last mobber less often than and P<0.025 for trial 2; r,= -0.64 and P<0.05 expected. for trial 3; r,= -0.30 and P<0.025 for combined trials). Comparison among Group Members During the experimental mobbing trials, fledglings responded to mobbers in several ways: The means and standard errors of the per cent- becoming quiet and motionless were seen once each time-mobbed, latency and closest approach are (jays of 51 and 56 days) and hiding was seen only in shown in Fig. 4. The data for different scrub jays two siblings of 51 days. Five fledglings slowly within a group were compared statistically with the approached while watching the adults mob and 11 Wilcoxon test. Male breeders mobbed a signifi- moved farther from the snake when mobbing cantly larger percentage of the time than did female began. In nine cases, the fledglings hopped about breeders in trial 1 (N=15, P<0.047), mobbed rapidly in trees or on the ground, without either more than helpers in trial 3 (N---7, P = 0.023), and approaching or retreating. Of the 34 fledglings that mobbed more than fledglings did in all trials responded to mobbers, 29 simply watched by (N=12 and P=0.008 for trial 1, N=12 and perching quietly. The percentage of fledglings that P=0"026 for trial 2, N= 13 and P---0.005 for trial responded to mobbers decreased from 67-6% in 3, N= 15 and P < 0.024 in all trials combined). No trial 1 to 32"0% in trial 2 and 20"0% in trial 3. A significant differences existed in per cent-time- significant negative correlation exists between the mobbed between female breeders and helpers. per cent-time-responded and fledgling age when the Female breeders mobbed more than their fled- Francis et al.." Florida scrub jay mobbing 807

Table III. Observed and expected number of times jays were the last mobber in the group

Number of groups Observed Expected

Trial 1 Male breeder 13 5 4,3 Female breeder 11 5 3,5 Mate helper 9 2 2.1 Female helper 4 3 0.7 Fledgling 12 4 5.0 Trial 2 Male breeder 9 3 2.8 Female breeder 8 3 2-1 Male helper 7 2 1,4 Female helper 6 1 1.0 Fledgling 11 4 4-7 Trial 3 Male breeder 11 6 3.2 Female breeder 8 1 2.3 Male helper 6 0 1.5 Female helper 5 0 1-1 Fledgling 11 4 4,2

IOOF 120~ 27 3001- 27 80~'/V=17 I li~ 4~ F-I~ ~or- ,~m t

~ I I 1-1 or'~Zl I Ol i i i I I Trial I

'~17680 ~..,V= 12 ,~ "~ ,~oI 9 g 2oo~- ~rn~ 2~ .9

0 0 ~ ' ~-' '~0 ~ ~ ~ JII- ~ I Trial 2

i00[-80LN:I3 120 I 500~ II

4~~oL 1- I I.-4-, 12 15 80p li 13 ,oTrl I o o I N~I-~I I -I~1 dB 9B H F dB s H F da C2B H F Trial 5

Figure 4. Bar graphs of the means of per cent-time-mobbed, latency and closest approach for trials 1, and 3. In each graph the data (from left to right) are from male breeders, female breeders, helpers and fledglings. 808 Animal Behaviour, 38, 5 glings in trial 1 (N=10, P=0.032) and overall Although the fledglings mobbed less intensely (N= 15, P < 0"005) and helpers mobbed more than than adults overall, by the third trial they differed fledglings in trial 2 (N= 7, P = 0,023). only from male breeders, and in one category only: Male breeders began to mob significantly sooner per cent-time-mobbed. Both helpers and female after the snake was detected by the group than did breeders also differed from the male breeders in this their mates in trial 3 (N-~ 6, P = 0.047) and overall category, so the fledgling mobbing behaviour was (N= 10, P=0.024), with results bordering on sig- very similar to adult mobbing behaviour by mid- nificance in trial 1 (N= 11, P=0-051). The male August. breeders also had a shorter latency than helpers when the trials are combined (N=6, P<0.047), Performance of Action Patterns and a shorter latency than fledglings in all but the third trial (N = 9 and P = 0-004 for trial 1, N = 9 and The 10 action patterns described previously did P<0.05 for trial 2, N= 10 and P=0.024 overall). not occur with enough regularity for a statistical Again, no differences existed between female comparison among group members. However, the breeders and helpers, but female breeders began combined data from the three trials are compared mobbing sooner than fledglings in trials 1 (N= 7, numerically in tables, as follows. P=0.023) and 2 (N=6, P=0-016). A non-signifi- Table IV lists occurrences of those action pat- cant tendency for helpers to have a shorter latency terns presumed not derived from incipient move- than fledglings occurred in trial 1 (N=5, ments of flight. These patterns, indicating strength P=0.063). of mobbing, were most common in breeders, then Male breeders approached the snake more clo- male helpers, and least common in female helpers sely than female breeders in trial 1 (N=12, and fledglings. Table V shows occurrences of action P<0.005), in all trials combined (N=12, patterns that are probably derived from incipient P = 0.008), and possibly in trial 2 (N = 7, P = 0.055). movements of flight, indicating fear of the snake. The closest approach of male breeders was also The patterns were most common in fledglings shorter than that of fledglings in the first (N= 9, followed closely by female helpers. P=0,006) and second (N=9, P=0.014) trials. All differences between male or female breeders and Changes in Individuals between Trials helpers in the closest approach were non-significant. Female breeders approached the snake more To determine whether mobbing changed over closely than fledglings in trial 1 (N=7, P<0,055) trials, relative cumulative frequency curves were and helpers approached more closely than fled- plotted. Cumulative frequency curves, unlike fre- glings in combined trials (N= 7, P= 0-039). quency histograms, avoid the blurring of data that

Table IV. Number and percentage of individuals that performed action patterns not derived from incipient movements of flight

Action pattern % Individuals that Mobbing Binocularly Orient Peck Bite performed at least Jay class call fixate toward perch snake Total N one action pattern

Male breeder N 38 11 9 4 4 66 (n=41) % 92.7 26.8 22.0 9.8 9-8 100 Female breeder N 31 6 4 1 0 42 (n=33) % 93.9 18.2 12.1 3.0 0 100 Male helper N 19 7 2 0 0 28 (n = 20) % 95.0 35.0 10.0 0 0 95.0 Female helper N 10 8 0 0 0 18 (n = 13) % 76.9 61.5 0 0 0 84-6 Fledgling N 42 31 14 2 0 89 (n=62) % 67.7 50.0 22.6 3.2 0 85.5 Total N 140 63 29 7 4 243 Francis et al.: Florida scrub jay mobbing 809

Table V. Number and percentage of individuals that performed action patterns derived from incipient movements of flight

Action pattern % Individuals that Flick Extend Flick performed at least Jay class tail upward Jump Bob wings Total N one action pattern

Male breeder N 4 1 1 4 0 10 (n=41) % 9.8 2.4 2.4 9.8 9 19.5 Female breeder N 5 0 0 3 1 9 (n=33) % 15.2 0 0 9.1 3.0 21.2 Male helper N 1 2 1 0 1 5 (n = 20) % 5.0 10.0 5.0 0 5.0 10.0 Female helper N 2 1 1 1 1 6 (n=13) % 15.4 7.7 7.7 7-7 7.7 38.5 Fledgling N 11 16 10 4 2 43 (n = 62) % 17.7 25.8 16.1 6.5 3.2 46.8 Total N 23 20 13 12 5 73

(a) (b) '~176F J

,. f,o'"

, , , , I ~ , , , I >~ o" ' ' ' ' ' ' ' ' ' ' "B (c) (d)

F . / .... o1:.....

~"g N=IS, 12,12 •lil•"•P" /V= 33, 25, 15 , , , I ~ , , n I , , , , I , , , , I 0 50 I00 0 50 I O0 Per cent-time-mobbed

Figure 5. Relative cumulative frequency (expressed as a percentage) of per cent-time-mobbed for male breeders (a), female breeders (b), helpers (c) and fledglings (d). first trial; o---o: second trial O---O: third trial. 810 Animal Behaviour, 38, 5

(a) (b) I00 ;~...~, ___~ ...... e r 5O

N=I7, II, 13 N=L2,9,11 g 0 , I I I I I i I , I , I I 1 i I i I i I (cl (d IOO 437 ~..:. ,,,..,,....:.~r....'n'..'n ."Z. -~ -"-'" "'~_~/~5 8 8 # ..:'r o~176176

N=13,11,7 N = 27, 22, 13

I i I i I i I ,~Jli. I I I I I I , I I I i I t.-I ii It 50 I00 150 200 >200 50 I00 150 200 250 300 >500 Latency (s)

Figure 6. Relative cumulative frequency of latency. See legend to Fig. 5.

(a) (b) ...... IO0 I ~ ll/- X' I ;" F.,~s~ I ,,..Y.. N=I7, II, 13 ~d N= 3,9,11 I i I , I i I I i I , I , I i I I I i 0 ~- (c) (d) I00 J~i~--~ ~.o.~ 518

.~_ /!"o, o,,~176 ~- 50 I

Ill" N=14,11,7 N=27,22, 13 i I , I , I ~ l;il~ I i I I I I ' i J I i I , 17,~ 0 100 200 300 400>400 100 200 ;500 400 500 600 700 >700 Closest approach (cm)

Figure 7. Relative cumulative frequency of closest approach. See legend to Fig, 5. Francis et aL: Florida scrub jay mobbing 811

(o) (b) I 00 .~ ,~..~ ~.o~//o ...... ~. ~'~4"~--~ -'~ 784 .,"" .O"

~ 50 .~ J /

~ ~ A/=I7,12, I5 ~.,,6 N=15,10,12 0 -' t , J , I ~ I , I , I//..I I I I I i J ' I I I I

=~ (c) (d lOOr ? [ .,/'782 .....e ~O~,D

[ Z

=33, ~5, L5 , 1 , t ,N=11"5'12'112 I I t I I i I I i I , I 0 100 200 300 400 500 600 >600 0 100 200 300 400 500 600 Time mobbed (s)

Figure 8. Relative cumulative frequency of time mobbed. See legend to Fig. 5.

(Q) occurs when values are grouped into categories; Io0 steeper curves reflect lower mean values. The data for the per cent-time-mobbed are presented in Fig. 5. For the breeders, the curves of the three trials are similar, and no significant changes occurred in 5O individual breeders. For the helpers, a simulta- neous comparisons of the three trials shows that the decrease from trials 1 to 3 is significant /V =54, 21, 14 (Friedman two-way analysis of variance, N=8, ?= two-tailed P<0.018), with trial 3 significantly a) 2- 50 IOO lower than trial 1 (N = 8, P = 0-0195). Although the Per cent-time-responded (b) three fledgling curves appear similar, these young O 100 ' .,o ...... o .._~//,o jays mobbed more in trial 2 than in trial 1 (N= 18, P < 0.049). A high frequency of short latency periods exists in all classes of jays and in all trials, with long latencies being relatively uncommon (Fig. 6). None 50 of the jay classes showed a significant change in latency between trials. Closest approach (Fig. 7) increased from trials 1 to 2 in male breeders (N = 9, N = 28, 18, 14 P<0.055) and in female breeders (N=8, I I I 1 I I I I I I I IMA.I P=0-0078). No statistically significant changes 0 2-5 5"0 >6"0 Per cent- time- responded/ occurred in helpers or fledglings, but there is an Per cent-time-mobbed indication of the same kind of change in helpers as occurred in adults. Note that fledglings actually Figure 9. Relative cumulative frequency of per cent-time- decreased their closest approach in repeated trials, responded (a) and of per cent-time-responded/per cent- reflecting development of more adult-like beha- time-mobbed (b) for fledglings.See legend to Fig. 5. viour. With respect to actual mobbing time (Fig. 8), 812 Animal Behaviour, 38, 5 male breeders decreased between trials 1 and 2 Table VI, one can assign ranks to each class of jays (N---10, P=0.027). Female breeders, helpers and within a given column. For example, male breeders fledglings showed no difference in mobbing time had the highest value of per cent-time-mobbed among trials. In per cent-time-responded, which than any other class so are assigned the top rank exists only for fledglings (Fig. 9), the fledglings (4); female breeders and helpers tie for the next decreased between trials 1 and 2 (N=14, highest value so they get the average middle rank P<0.0043) and between trials 1 and 3 (N=10, (2.5); and fledglings get the lowest rank (1). These P=0'0049). Similarly, the per cent-time-res- ranks for each jay class are summed to give a total ponded/per cent-of-time-mobbed decreased from which is an overall index of mobbing intensity. trials 1 to 2 (N= 10, P<0.0049). Only fledglings Male breeders have the highest sum ranking as high exhibited a change in the likelihood of discovering as or higher than other jays in all cases. Female the snake. Individual fledglings were more likely to breeders scored higher than helpers in the latency discover the snake in trial 2 than in trial 1 and in action patterns not related to flight, but they (P=0'035, Friedman two-way analysis-of-vari- scored lower in closest approach. As a result, the ance, two-tailed). mobbing intensities of female breeders and helpers are similar. Summary of Comparisons Table VI provides an overall summary of family comparisons for the entire season. Focusing on The upper section of Table VI gives a summary changes over time, the null hypothesis that fled- of how group members compare with one another gling mobbing intensity should not increase with in mobbing intensity. Biting the snake is listed time was rejected with respect to per cent-time- separately because biting involves physical contact mobbed and -responded, and the ratio of these two with the snake and presumably entails more risk variables. Also, fledglings became more likely to than other action patterns, but the other four discover the snake as they matured. For adults, the action patterns not related to flight are combined. null hypothesis that mobbing intensity should not Based on the summary of ordered comparisons in change was rejected only with respect to closest

Table VI. Summary of comparison of group members and ranks of mobbing intensity

Per cent- Other non- Flight- time- Closest Bite flight action derived action mobbed Latency approach snake patterns patterns Comparison Male versus > > > > = = female breeder Male breeder > > = > > = versus helpers Female breeder .... > = versus helpers Male breeder > > > > > > versus fledglings Female breeder > > > = > > versus fledglings Helpers versus > = > = > > fledglings Ranks Sum of ranks Male breeder 4 4 4 4 3.5 3 22.5 Female breeder 2.5 3 2 2 3.5 3 16-0 Helpers 2.5 2 3 2 2 3 14.5 Fledglings 1 l 1 2 1 1 7.0

> : first member of the pair mobs more intensely than the second. = : the two members show no difference in mobbing intensity. Francis et al.: Florida scrub jay mobbing 813 approach in female breeders and absolute mobbing Barkan et al. (1986) found that male grey- time in male breeders. Although fledglings mobbed breasted jays, Aphelocoma ultramarina, a congener less than adults when all the trials are combined, by of the scrub jay, had a tendency to be dominant in the third trial their mobbing behaviour differed social interactions, and discuss the problem of little from that of female breeders and all helpers. sexual asymmetries. It is apparently not known if In some ways fledgling behaviour changed while male grey-breasted jays are stronger mobbers than adult behaviour remained constant (in the per cent- females (see Cully & Ligon 1976). time-mobbed and detection of the snake), and in Slagsvold (1984) found that one individual others some of the adults changed while the hooded crow, Corvus corone cornix, acted as a fledglings did not (closest approach and absolute 'leader' in mobbing a stuffed owl, and in fact chased mobbing time). These differential changes in beha- away other crows. He interpreted mobbing as 'self- viour would account for the mobbing by the young advertisement' rather than anti-predator defence. jays becoming more adult-like. In a later study Slagsvold (1985) found the mobbing 'leader' to be an adult male crow, 'probably also the dominant bird in the flock hierarchy'. We DISCUSSION have never seen the breeding male scrub jay chase Sexual Asymmetry any member of its group during mobbing. Still, it seems possible that the breeding male's more Male and female Florida scrub jays are morpho- intense mobbing (Table VII), including biting the logically similar (Woolfenden 1978) and in many snake, might play some role in demonstrating his ways behaviourally similar. They are permanently abilities to other members of the group, thus monogamous and permanently territorial and both reinforcing his dominance status. sexes care for the young (Woolfenden & Fitzpa- Payne et al. (1985) found that in the cooperati- trick 1984). The death rates of breeders (but not vely breeding, group-living splendid wren, Malurus helpers) are equal for the sexes (Fitzpatrick & splendens, the breeding female was usually the first Woolfenden 1988). Despite these similarities sexual to detect and attack a stuffed cuckoo (which is a asymmetries pervade the social system of Florida nest-parasite, not a predator). The stuffed cuckoo scrub jays. Among all mature jays, males dominate was set near the nest, more frequently visited by the females, and among breeders, males respond to breeding female than other individuals. All other territorial intrusions more quickly than their mates group members responded about equally, It seems (Woolfenden & Fitzpatrick 1977) and males per- likely that which class of birds of a group detect a form sentinel duty more often than do their mates predator first and mob it most intensively depends (McGowan & Woolfenden 1989). Males deliver upon the species of mobber, perhaps the species more food to nestlings (Stallcup & Woolfenden mobbed, and the context of the behaviour. 1978), while only females incubate and brood (Hailman & Woolfenden 1985). Among pre- breeders, males remain as helpers longer than Roles of Helpers females, and they deliver more food to nestlings As the mobbing behaviour of helpers is similar to (Stallcup & Woolfenden 1978). Males regularly that of female breeders (though less than that of become breeders in a segment of the territory they male breeders), it seems likely that helpers contri- occupied as helpers; females rarely do (Woolfenden bute significantly to the anti-predator behaviour of & Fitzpatrick 1978, 1984). Females disperse earlier the group. They may increase the reproductive and farther to become breeders (Woolfenden & success of the breeding pair by decreasing the rate Fitzpatrick 1986). of predation on the breeders, eggs, nestlings and To these differences we now add sexual asymme- fledglings (Stallcup & Woolfenden 1978; Woolfen- tries in mobbing. Among breeders, males mob den 1978; Wootfenden & Fitzpatrick 1984). This longer and approach snakes more closely than do study shows that helpers are an important part of females, and also more closely than do helpers and the anti-predator behaviour of the group, It seems fledglings. Only breeding males were seen to attack likely that mobbing decreases the probability that a the snakes. A similar trend is evident among pre- predator will successfully capture prey, although of breeders (Table IV), although the difference is not course mobbing does not always succeed in pre- statistically significant. venting predation (see Lohrer 1980; Webber 1980). 814 Animal Behaviour, 38, 5

Possible mechanisms for reducing the probability mobbing call given by an adult. A similar situation of successful predation in other birds have been exists in Belding's ground squirrels, Spermophilus discussed by Curio (1978). A scrub jay group with beldingi, where alarm calls by juveniles often elicit helpers is more likely to avoid predation than a no response from adults (Robinson 1981). Aerial group without helpers, for at least two reasons. predator alarm calls are given by scrub jay fled- First, the larger the number of group members that glings at times when a predator is not apparent have had experience with predators, the more likely (Barbour 1977). The trend for male helpers to do that a predator will be detected before it can more mobbing than female helpers (Table IV) is capture a jay. Second, if mobbing serves to deter a not statistically significant but may be real. If so, it predator on at least some occasions, it is plausible probably reflects the sexual asymmetries estab- that a larger number of mobbers would be more lished for breeding adults. successful in doing so.

Social Structure and Mobbing in Jays Ontogeny of Mobbing Cully & Ligon (1976) found that the mobbing of Fledglings gradually acquire the mobbing beha- a tethered great horned owl by western scrub jays viour typical of adults over a period of about 2 and grey-breasted jays differed in several ways. The months. This is about the same developmental group-breeding grey-breasted jays formed mob- course as shown in sentinel behaviour (McGowan bing assemblages (composed of group members) 1987). Fledglings younger than at least 33 days do quickly, mobbed for 35-45 rain, and often returned not mob. Rather, they become silent and motion- to mob again after temporarily leaving the area. less when adults give mobbing calls. Buitron (1983, Western scrub jays formed mobbing assemblages page 225) reports similar behaviour in fledgling (composed of neighbouring pairs) more slowly, black-billed magpies, Pica pica: 'young out of their mobbed for 15-20 rain, were less likely to mob nest for several days typically responded to an again after leaving, seemed to be distracted by alarm rattle by immediately moving out of sight other mobbers (probably territorial intruders), and and remaining silent for several minutes'. maintained individual distances (between jays) of Eventually the fledglings begin to join their about 1 m. groups in mobbing snakes. This critical age seems While mobbing the experimentally presented to be between 33 and 47 days although some older snake, Florida scrub jays quickly formed mobbing fledglings also did not mob. Development may be assemblages (composed of group members, some- more rapid in the black-billed magpie, as Buitron times including neighbouring fledglings but only (1983, page 225) reports that 'within two weeks [of rarely neighbouring adults), often recommenced fledging] fledglings began joining their parents in mobbing after temporary lulls, and were disturbed rattling, and would help harass crows and coyotes'. by other mobbing jays only when they were adults Young scrub jays are first able to fly about 2 weeks ofneighbouring territories. In several ways Florida after fledging, at around 31 days of age. The ability scrub jay mobbing behaviour is thus similar to that to avoid predation through improved flying and of grey-breasted jays. The rapid formation of a terrestrial locomotion may be the critical factor mobbing group and the close proximity ofmobbers needed before jays begin to mob predators. Fled- in Florida scrub jays and grey-breasted jays prob- glings between 30 and 40 days old are still awkward ably result from a social system in which the social in the air; whereas, by 47 days, the youngest age unit consists of a group of at least several indi- group known to mob, they are much more coordi- viduals (Cully & Ligon 1976). An interesting nated in flight. After this point they are able to difference between western and Florida scrub jays approach a snake with much less risk of predation. is that western scrub jays were more tolerant of When fledglings discover snakes and initiate neighbouring pairs during mobbing whereas Flor- mobbing, they are often ignored by adults; mob- ida jays interrupted mobbing to repel adult terri- bing adults are never ignored. It may be that a torial intruders. However, this difference might be mobbing call given by a fledgling is less likely to be related to type of predator used in trials (owl and associated with the appearance of a predator than a snake, respectively) rather than social structure. Francis et al.: Florida scrub jay mobbing 815

ACKNOWLEDGMENTS Daanje, A. 1951. On locomotory movements in birds and the intention movements derived from them. Beha- viour, 3, 48-98. We thank James N. Layne for making available the Fitzpatrick, J. W. & Woolfenden, G. E. 1988. Compo- facilities at the Archbold Biological Station and his nents of lifetime reproductive success in the Florida notes on species of snakes mobbed by Florida scrub scrub jay. In: Reproductive Success (Ed. by T. H. jays. This research was partially funded by a Davis Clutton-Brock), pp. 305-320, Chicago: University of Fund travel fellowship from the Zoology Depart- Chicago Press. Gross, A. O. 1949. Nesting of the Mexican jay in the ment at the University of Wisconsin-Madison, and Santa Rita mountains. Condor, 51, 241 249. the senior author was supported by a National Hailman, J. P. & Woolfenden, G. E. 1985. Nest-defense in Science Foundation Graduate Fellowship. Further the Florida scrub jay and the problem of 'incubation' in support came from N.S.F. grant BNS-83t6001 to male passerines. Wilson Bull., 97, 370-372. Hardy, J. W. 1961. Studies in behavior and phylogeny of J.P.H. We thank Cheryle Hughes (who prepared certain New World jays (Garrulinae). U. Kans. Sci. the illustrations), Jeffrey R. Baylis, William H. Bull., 42, 13-149. Buskirk and Kevin J. McGowan (who critically Hinde, R. A. 1952. The behaviour of the great tit (Parus reviewed the initial manuscript), and Richard L. major) and some other related species. Behav. Suppl. 2, Knight and A. Margaret Elowson (who reviewed 1-201. Hinde, R. A. 1954. Factors governing the changes in the revision). We are also indebted to W. John strength of a partially inborn response, as shown by the Smith and an anonymous referee for further criti- mobbing behaviour of the chaffinch (Fringilla coelebs). cism. II. The waning of the response. Proc. R. Soe. Lond., Set. B, 142, 331-358. Lohrer, F. E. 1980. Eastern coachwhip predation on REFERENCES nestling blue jays. Fla Field Nat., 8, 28-29. McGowan, K. J. 1987. Social development in young Altmann, S. A. 1956. Avian mobbing behavior and Florida scrub jays (Apheloeoma c. eoerulescens). Ph.D. predator recognition. Condor, 58, 241-253. thesis, University of South Florida. Amadon, D. 1944. Results of the Archbold expeditions, McGowan, K. J. & Woolfenden, G. E. 1989. A sentinel no. 50: a preliminary life history study of the Florida system in the Florida scrub jay. Anim. Behav., 37, 1000- jay, Cyanocitta c. coerulescens. Am. Mus. Novit., 1252, 1006. l 22. Mumme, R. L. 1987. Eastern indigo snake preys on Barbour, D. B. 1977. Vocal communication in the Florida juvenile Florida scrub jay. Fla Field. Nat., 15, 53-54. scrub jay. M.A. thesis, University of Florida. Payne, R. B., Payne, L. L. & Rowley, I. 1985. Splendid Barkan, C.P.L., Craig, J. L., Strahl, S. D., Stewart, A. M. wren Malurus splendens response to cuckoos: an experi- & Brown, J. L. 1986. Social dominance in communal mental test of social organization in a communal bird. Mexican jays Aphelocoma ultramarina. Anita. Behav., Behaviour, 94, 108-127. 34, 175-187. Robinson, S. R. 1981. Alarm communication in Belding's Brown, J. L. 1963. Social organization and behavior of ground squirrels. Z. Tierpsychol., 56, 150-168. the Mexican jay. Condor, 65, 126-153. Rohlf, F. J. & Sokal, R. R. 1969. Statistical Tables. San Brown, J. L. 1970. Cooperative breeding and altruistic Francisco: W. H. Freeman. behaviour in the Mexican jay, Alphelocoma ultramar- Siegel, S. 1956. Nonparametric Statistics for the Beha- inc. Anim. Behav., 18, 366 378. vioral Sciences. New York: McGraw-Hill. Brown, J. L. 1972. Communal feeding of nestlings in the Slagsvold, T. 1984. The mobbing behaviour of the Mexican jay (Aphelocoma ultramarina): interfiock com- hooded crow Corvus corone cornix; anti-predator parisons. Anita. Behav., 20, 395-403. defence or self-advertisement? Fauna norv. Ser. C, Brown, J. L. 1974. Alternate routes to sociality in jays-- Cinclus, 7, 127-131. with a theory for the evolution of altruism and Slagsvold, T. 1985. Mobbing behaviour of the hooded communal breeding. Am. Zool., 14, 63-80. crow Corvus corone cornix in relation to age, size, Buitron, D. 1983. Variability in the responses of black- season, temperature and kind of enemy. Fauna norv. billed magpies to natural predators. Behaviour, 88, Ser. C, Cinclus, 8, 9-17. 209-235. Smith, H. M. & Brodie, E. D., Jr. 1982. Reptiles of North Conant, R. 1975. A Field Guide to Reptiles and Amphi- America. New York: Golden Press. bians of Eastern and Central North America. Boston: Stallcup, J. A. & Woolfenden, G. E. 1978. Family status Houghton Mifflin. and contributions to breeding by Florida scrub jays. Cully, J. F,, Jr & Ligon, J. D. 1976. Comparative Anim. Behav., 26, 1144-1156. mobbing behavior of scrub and Mexican jays. Auk, 93, Webber, T. A. 1980. Eastern coachwhip predation on 116-125. juvenile scrub jays. Fla Field Nat., 8, 29-30. Curio, E. 1978. The adaptive significance of avian Westcott, P. W. 1970. Ecology and behavior of the mobbing. I. Teleonomic hypotheses and predictions. Florida scrub jay. Ph.D. thesis, University of Florida. Z. Tierpsychol., 48, 175-183. Woolfenden, G. E. 1973. Nesting and survival in a 816 Animal Behaviour , 38, 5

population of Florida scrub jays. Liv#tg Bird, 12, Woolfenden, G. E. & Fitzpatrick, J. W. 1984. The Florida 25-49. Scrub Jay: Demography of a Cooperative-breeding Bfi'd. Woolfenden, G. E. 1975. Florida scrub jay helpers at the Princeton, New Jersey: Princeton University Press. nest. Auk, 92, 1 15. Woolfenden, G. E. & Fitzpatrick, J. W. 1986. Sexual Woolfenden, G. E. 1978. Growth and survival of young asymmetries in the life history of the Florida scrub jay. Florida scrub jays. Wilson Bull., 90, 1-18~ In: Ecological Aspects of Social Evolution (Ed. by D. I. Woolfenden, G. E. & Fitzpatrick, J. W. 1977. Dominance Rubenstein & R. W. Wrangham), pp. 87 107, Prince- in the Florida scrub jay. Condor, 79, 1-12. ton, New Jersey: Princeton University Press. Woolfenden, G. E. & Fitzpatrick, J. W. 1978. The inheritance of territory in group-breeding birds. Bio- (Received 18 May 1988; revised 14 November 1988; Science, 28, 104-108. MS. number: A5307)