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Behav Ecol Sociobiol (2003) 53:287–296 DOI 10.

1007/s00265-002-0571-2

O R I G I N A L A RT I C L E

Hugh Drummond · Cristina Rodríguez Adriana Vallarino · Claudia Valderrábano Gabriela Rogel · Emilio Tobón

Desperado siblings: uncontrollably aggressive junior chicks
Received: 31 May 2002 / Revised: 2 December 2002 / Accepted: 4 December 2002 / Published online: 22 January 2003 © Springer-Verlag 2003

Abstract According to the desperado sibling hypothesis, chicks of obligately siblicidal species kill their junior broodmates as early as possible because junior broodmates face dire ecological prospects and are consequently predisposed to aggressively overthrow elder broodmates by all-out aggression. The agonistic behavior of junior chicks is virtually unknown because they die so young. We investigated the agonistic behavior of hypothetical desperados by fostering junior brown boobies (Sula leucogaster, an obligately siblicidal species) into nests of the blue-footed booby (S. nebouxii, a facultatively siblicidal species) containing an older singleton blue-foot chick. Controls were junior blue-footed boobies fostered into the same situation. Junior brown boobies were 7 times more aggressive than controls and most of them dominated their elder and larger nestmates. Four of nine brown booby juniors showed relentless aggression, delivering up to 711 pecks, bites and pushes (including “expulsion pushes”) per hour, thereby overwhelming nestmates 90% heavier and permanently expelling one of them from the nest. Similarly, in natural broods of two surviving brown booby chicks, the losing chick was 13 times as aggressive as blue-foot subordinates, up to at least age 7 weeks. Contrast of the two species of booby suggests the evolution of agonistic roles within broods may be partly driven by selection on potential victims to express a level and type of aggressiveness appropriate to their status-related ecological prospects. Keywords Aggression · Brood · Desperado · Siblicide · Sibling

Introduction
Why do some birds kill their infant siblings as early as they are apparently able? Among species whose chicks compete aggressively for dominance and access to parentally provided food, there is a minority of species that frequently hatch two chicks, only for one of those chicks routinely to dispatch its broodmate within days of hatching. In this obligate siblicide, the senior (elder) chick repeatedly pecks, pushes and bites at the broodmate until it eventually succumbs through lesions, starvation or expulsion from the nest (reviews in Mock 1984; Bortolotti 1986; Anderson 1990; Mock and Parker 1997). Although in several facultatively siblicidal species aggression of the elder chick has been shown by experiments to vary with food deprivation and other factors (reviews in Mock and Parker 1997; Drummond 2001a, 2001b), in obligate siblicide aggression usually appears urgent and unconditional, and indeed occurs despite apparently adequate food provision by parents (e.g., Meyburg 1977; Gargett 1978; Gerhardt et al. 1997). According to the insurance hypothesis (Dorward 1962; Mock and Parker 1986; Clifford and Anderson 2001), even if parents are incapable of provisioning two offspring all the way to independence, they and their senior offspring could often gain in fitness by nurturing or tolerating the junior chick for a while lest it be needed to substitute a senior chick that proves inviable or suffers predation. Stinson’s (1979) notion of “pending competition” explains why it may be adaptive to dispatch a sibling even when parental provision is currently sufficient for the two hatchlings: if the developing brood of two will inevitably outstrip the food supply, then one chick will in the end have to be sacrificed (see also Forbes 1990; Forbes and Ydenberg 1992). This notion explains the occurrence and the apparent unconditionality of obligate siblicide, but it does not explain the timing and the urgency. These features may be explained by the “desperado sibling” hypothesis (Drummond 1993), derived from Stinson’s (1979) insight that a junior chick can potentially grow to outcompete its initially dominant sibling and

Communicated by C. Brown H. Drummond (✉) · C. Rodríguez · A. Vallarino C. Valderrábano · G. Rogel · E. Tobón Instituto de Ecología, Universidad Nacional Autónoma de México, A.P. 70–275, 04510 D.F., Mexico e-mail: hugh@servidor.unam.mx Tel.: +52-5-6229007, Fax: +52-5-6228997

1. Apparently. On Isla Isabel. allowing the evolution of broodmate agonism to be driven partly from below. We fostered young junior chicks of the brown booby into one-chick nests of the facultatively siblicidal bluefooted booby. Evans’ (1996) observations of an obligately siblicidal population of white pelicans (Pelecanus erythrorhynchos) showed a high probability of junior chicks surviving through the period when most senior chick deaths occurred (senior ages 0–7 days). but on San Pedro Mártir 65% of junior chicks were dead within a week. not only because they spend most of their brief lives concealed under the parent but also because when visible they are often overwhelmed by a barrage of attacking and because their evasions or struggles command less attention than the dramatic violence of their siblings. and the youngest chick consequently is a designated victim with near zero prospects of surviving to breed.288 Grafen’s (1987) desperado concept. Tershey et al. but exceptionally two chicks may fledge. confronted by a competitor disposed to launch an all-out assault. during the period when they could be called on to provide insurance benefit (Evans 1996). respectively. Parents may well adjust the hatching interval to ensure that junior chicks perish at the age when senior chicks are safe. The agonistic behavior of junior chicks of obligate siblicide species is largely unknown. 2000). The senior brown booby chick’s agonistic advantage derives from a large initial difference in size and maturity. Nuechterlein 1981) to fighting back and even initiating fighting in great egrets (Casmerodius albus) and brown pelicans (Pelecanus occidentalis) (review in Drummond 2001a). Consequently. provided apparent insurance benefit by giving rise to the sole fledgling of the nest (Woodward 1972. 15% and 12% of second eggs. The proportion of deaths and age of mortality in two-chick broods have seldom been quantified. biting and pushing. valuable insurance is discarded prematurely. 2000). the b-chick would already be dead. should eliminate the emerging threat as soon as possible. In contrast. 16%. thereby providing each brown booby with . Tershey et al. although it is not clear how much of this benefit accrued through loss of the senior sibling at the egg versus chick stages. Drummond and Canales 1998) and western grebe (Aechmophorus occidentalis. In turn. the prospect of an attempted coup by the junior chick obliges the senior chick to prematurely discard (1) the family’s insurance against first chick failure and (2) whatever (slim) possibility exists of fledging two chicks. (2000) considered that the brown booby on San Pedro Mártir is not obligately siblicidal because 7% of two-egg clutches gave rise to two fledglings. so intense selection on chicks to compete for survival could in principle drive the age of death to a lower value than suits parental interests. due to broodmates hatching an average 4. and when senior chicks were experimentally removed from nests when their junior broodmates were 3 or 6 days old. On Kure Atoll.6±0. In the expanding population of Johnston Atoll.g.5 days by their broodmates’ round-theclock pecking. we studied chicks of the brown booby (Sula leucogaster). and whose relative aggressive prowess increases by the day. The desperado sibling hypothesis applies to species where parents can seldom or never provision the whole brood all the way to fledging.4% of clutches produced two fledglings each and on San Pedro Mártir 7% of two-egg clutches that fledged any chicks at all fledged two chicks (to the age when they were nearly fully feathered). where brown booby broods were watched 24 h per day. In this situation. by selection on the behavior of the designated victim. Another hypothesis for the timing of obligate siblicide holds that parents calibrate the hatching interval (and hence the agonistic asymmetry) of their brood so that killing of the junior chick is guaranteed (Simmons 1988. parents probably cannot control the behavior of their offspring completely (Trivers 1974). Evans (1996) calculated that there was a 14% chance that when required to replace a failed a-chick. a groundnesting species that generally lays one or two eggs and often hatches two chicks but rarely raises both of them to independence because the junior one regularly falls victim to broodmate aggression (review in Nelson 1978). that is. but Simmons (1988) and Anderson (1990) considered that siblicide is obligate where fewer than 10% of junior chicks survive. However. 21% of those juniors proved to be already too weakened by sibling harassment and starvation to survive even as singletons (Evans 1997). starvation and exposure resulting from broodmate attacks and eviction (Tershey et al. all junior chicks that survived predation were killed within 6.17 days (mean±SE) apart (Cohen Fernández 1988). Amerson and Shelton 1976 in Nelson 1978. his more detailed observations imply that the death or lethal debilitation of junior chicks in that population often occurs when parental interests would require continued survival: half of junior pelican chicks died at ages 0–6 days. attempting to overthrow and displace the more powerful competitor is a strategy that carries negligible cost and should be favored by selection if the chick has the physical wherewithal to use violence effectively. and it varies greatly from conditional acceptance of subordination in the blue-footed booby (Drummond and Osorno 1992. Anderson 1989) and does not occur until after the age when senior chick survival is assured and insurance is no longer needed (Evans 1996). The insurance hypothesis seems to account for laying of a second egg by this species (Dorward 1962). However. O’Connor 1978. and not before. Models of siblicide evolution frequently assume that a senior chick has sufficient control to kill its rival at its own convenience (at least when unopposed by parents) and that the junior chick is debarred from killing by physical inferiority (e. To test the desperado sibling hypothesis. Johnston Atoll and San Pedro Mártir Island. the desperado sibling hypothesis proposes that siblicide can be an option for junior chicks. the senior chick. In facultatively siblicidal species the agonistic behavior of junior chicks is somewhat better known (although seldom the focus of attention). evidently due to injuries. “runt” model in Godfray and Harper 1990).

Each trial started when the junior chick was removed from its home nest. the resident chick was removed.0±0. Setting the date the first trial started as 1. The observer sat 4–6 m from the focal nest without a blind (boobies with chicks are extraordinarily tolerant of human presence). Sex of chicks was not known. and expulsions (the victim is forced or flees across the perimeter rim of the nest).6±1. we fostered young junior blue-footed boobies into conspecific nests containing a single older chick.15 days and weighing 198±24. often until both birds become independent at about 4 months of age. Trials ended when we transferred the brown boobies back into a conspecific nest while they were still young enough to integrate into the family. (1986).1% heavier than its nestmate.77 days and weighing 104±12.5±0.88 and 3. Methods Fostering experiment The experiment was carried out in March 2001 on the island of San Pedro Mártir. and recorded the absolute frequency of pecks (impact of the bill on the victim). 112º20′W). it is likely that a minority of the singleton blue-footed booby chicks were survivors of two-chick broods reduced by junior chick death (or even senior chick death). although the youngest juniors were not observed until the second or third day after transfer (very young chicks are brooded and can seldom be seen). Junior brown boobies were scarce. yielding nine pairs in which the senior chick was 5.1 g. and non-submissive beyond temporary evasion and avoidance (Drummond 2001a). Junior blue-footed boobies can become aggressive if they detect weakness in their broodmate.7% heavier than the resident chick. The senior bluefooted booby chick is 4. The 11 experimental pairs were observed on 7. then declined more or less progressively between ages 3 to 9 weeks. pushes (the seized victim is displaced at least 1 cm by thrusting with the mandibles). allowing us to describe the agonistic behavior of a young brown booby chick confronted by a larger. using growth curves of blue-footed and brown boobies on Isla Isabel. which were transferred into blue-footed booby nests containing singleton chicks of age 13. yellow or blue acrylic paint (colors assigned haphazardly) for identification during observations.18 days and weighing 97±16. Observation started the day after transfer. at a time. starting when the junior chick was 8. Then both chicks were inserted simultaneously into the center of the nest and the “family” was watched to confirm acceptance of the chicks. We reasoned that a junior brown booby chick would probably survive longer in the nest of its congener. bites (the victim is seized in the mandibles for at least 1 s). when observation was suspended or reduced to 1. Each pair was watched every day for 3 h. start dates of experimental trials and control trials were 3. Experimental trials ended when we permanently transferred the brown booby junior to a conspecific nest containing a similar-sized chick. After some early beatings. We observed these nests for several days and confirmed that the foster chicks were accepted by the adults. For the control treatment. Provided it is adequately fed.84 days older and initially 91±12. measured (culmen). and their ages were estimated from culmen length. There.4±1. so we used all individuals aged 2–11 days for which an appropriate experimental pairmate could be found.4±1. the senior blue-footed booby chick in a twochick brood usually deploys only enough aggression to ensure the subordination of its broodmate and secure its own feeding priority (Drummond and García Chavelas 1989. Observers watched one pair. brown booby juniors should be uncontrollable: highly aggressive except when overwhelmed.3±1. The desperado sibling hypothesis predicts that in comparison with controls. we took advantage of the existence of natural surviving pairs of brown booby broodmates in the 2001 season. except for the four trials (two in each treatment) where the junior chick died earlier.9±1.7 g. which always occurred. 105º55′W). The desperado sibling hypothesis predicts that in maturing two-chick broods of the brown booby aggression by both broodmates should be more intense and decline less with age than in the blue-footed booby. the senior chick is a ‘trained winner’ and the junior chick is a ‘trained loser’ (Drummond and Osorno 1992. simply leaving the junior chick in its foster nest (to save it the challenge of reintegrating into the home nest). the chicks were weighed and measured. Anderson and Ricklefs 1995).10 days old. Although the identification of junior chicks was certain. Drummond and Canales 1998). The control subjects were nine blue-footed booby junior chicks of age 7. wrapped in cloth and transported (in less than 20 min) to the foster nest.4±0. in the Sea of Cortéz (28º23′N. starting when the junior chick was 8.3 g. and the 9 control pairs were observed on 7. Additionally. both chicks were weighed with a spring balance. Experimental and control trials ran during roughly the same dates. except on exceptional days when insufficient observers were available. Trials ended when the junior chick reached age 18 days. to make a comparison of agonism in maturing brown booby broods versus maturing bluefooted booby broods.4±0. At the end of each day’s observation.000 nests every 3–7 days.289 an elder nestmate expected to be less aggressive than a typical brown booby elder broodmate. Nelson 1978).27 days and weighing 209±33. older and more powerful competitor. aggression peaked at ages 10–20 days.9 g. alternating whenever possible between morning (0800– 1100 hours) and afternoon observations (1500–1800 hours) of each pair. exceptionally two pairs. and sought a similar-aged sample of blue-footed booby juniors for the control treatment. The experimental subjects were 11 brown booby junior chicks of age 7. The senior chick allows the junior chick to cohabit and share resources for several days or weeks.36 days older than its broodmate (Castillo and Chavez-Peón 1983). after an average 11 days cohabitation in the foster nest.65 days old.5 h.9±0.03. yielding 11 pairs in which the senior chick was 5. respectively. Chicks were selected for the experiment by surveying about 1. 1991). noting also for each . In blue-footed booby broods described by Drummond et al. Hence. fitted with a numbered plastic leg band and marked on the head and rump with red. but this probability was the same for experimental and control pairs.34 days.02 days. By this time.0±0. and their paint marks were renewed if necessary.8±0. the junior blue-footed booby broodmate largely renounces its attempts at aggression and routinely concedes to attacks and aggressive displays by adopting the submissive bill-down-and-face-away posture (BDFA. as nestmates continue striving to eliminate each other rather than adopting a relationship of dominance-subordination. because each one was found cohabiting with a larger broodmate. nearby in the Mexican Pacific Ocean (21º51′N.87 days older and 117±21.2±1. but they seldom manage to invert the dominance relationship (example in Drummond et al. which were transferred into blue-footed booby nests containing singleton chicks of age 12. Control trials ended when we suspended observation of the two nestmates. in both samples the average age difference between nestmates was slightly greater than the average difference in natural broods of the junior chick’s own species.

For analysis.008). Sample values are expressed as mean±SE throughout.204.07.3±2.6% (n=9) and 85±25. No exceptional behavior was observed in any of the four broods. and weights of the junior blue-footed boobies were similar to those of sameaged junior conspecifics on Isla Isabel (data not shown).4 ± 21. 1). Across the whole trial. using the same behavioral recording system used in the experiment. At that time.2±1. boobies were similar to those of same-aged conspecific singletons (including senior chicks whose broodmates had died) on Isla Isabel.459. respectively).9±2. The observer also recorded every half minute (signaled precisely by a bleep) whether each chick was inactive (head resting on any substrate or invisible under attending adult) or active in that instant. their nestmates (0. 0. 0. at ages 12 days and 15 days.755. measured (culmen) to estimate age and paint-marked for individual identification. was the brown booby’s main mechanism for evicting a broodmate. Recorded as a bite or push. it seems that the brown booby chicks were adequately cared for by blue-footed booby adults.01 acts per hour (robust rank order test. instead of sorting data by junior versus senior chick we sorted by dominant versus subordinate chick.230. All statistical tests were two-tailed and we compared median aggressive rates in independent samples with the robust rank order test (Hollander and Wolfe 1999) when unequal variances precluded use of the Mann-Whitney U-test (Kasuya 2001). The four deaths were similar to typical junior chick losses in the blue-footed booby and probably associated with junior status. with subordinate chicks 29–51 days old (40. Hence. together with more horizontal pushing with open or closed mandibles. walking forward. respectively. were performed by brown booby juniors (0. each of five observers searched the colony for broods of two chicks more than 4 weeks old. if possible.67 days) and 17 bluefooted booby broods with subordinate chicks 28–59 days old (43. U=−3.05. according to which broodmate performed more aggressive acts (we did not take submissive behavior into account).43 days).39.19 days) and the 17 dominant blue-footed boobies were 30–64 days old (46. respectively. 45. One of these brown booby juniors steadily lost weight over 5 days and was found dead on the nest. systematically grasping the rival’s body part (often the nape or wing) in its mandibles for several seconds while thrusting forcefully outward and upward and. The samples obtained were 16 brown booby broods.466. Brown booby juniors were individually active during an average 22% of the observation time and simultaneously active with their pairmates during 14% of the time.2% (n=7) larger than their junior nestmates. the 16 dominant brown boobies were 30–60 days old (42. and in 2 of 9 control pairs. weights of the junior brown . The maximum daily rates of the four individuals.015).025). 0. Hence. only the brown booby performed “expulsion pushing”. This last record was taken in order to determine how much of the time both pairmates were simultaneously awake and therefore available to interact (chicks sleep most of the time) and discriminate whether different frequencies of aggression were due to aggressiveness versus opportunity to attack. 31 and 81 aggressive acts per hour. and on the last day of observation the experimental and control seniors in pairs that suffered no mortality were 53±11. sometimes as far as several bodylengths and. considerably greater than the maximum values for the remaining seven brown booby juniors and the nine blue-footed booby juniors of 0.9 and 1. the junior chick never ceased attacking unless it was itself attacked. at times when both nestmates were simulta- Results Fostering experiment General The junior chick died before the end of the trial in 2 of 11 experimental pairs. the other gained weight normally and was found dead 15 cm from the nest. Aggression was mostly pecking. The two blue-footed booby juniors disappeared from the nest. one had been growing normally and the other had gained no weight in the last 3 days. All senior chicks remained larger than their foster nestmates throughout the trials. respectively.032). B78 and A55) forming a distinct subgroup marked by long bouts of attacking that was relentless in the sense that as long as both chicks were awake and the senior one was visible and within striking distance.013) and their nestmates (0. P<0. selecting the first observable brood or pair of broods encountered (later we discarded a few broods to make the samples of both species similar in age). 0. and a chick was considered dominant on any particular day if it performed more aggressive acts than its nestmate. and for blue-footed booby juniors the average percentages were similar (23% and 15%. this behavioral pattern functioned to displace the rival. rates of aggression are simply expressed per hour of observation except where otherwise noted. Fig. The maximum rates of aggression scored by these four individuals on any day were 64. bites and pushes were summed together as aggressive acts.501.3±1. individual variation in aggressiveness was great. blue-footed booby juniors (0. 0. 0. We could not reliably determine which broodmate was the elder since at these ages the larger body size of females confuses comparisons of unsexed birds. However. attacks. followed in frequency by biting and then pushing. Among the brown booby juniors. So. respectively. U=−2.689.290 peck whether the victim was submissive (adopted or sustained a BDFA posture).3–6. A similar difference was observed in rates of aggressive acts during times when both nestmates were simultaneously active: brown booby juniors were eight times as aggressive as blue-footed booby juniors.24 days). Chicks were captured by hand.427. B57. the following average proportions of those acts.0 aggressive acts per hour. Nayarít. Aggression of juniors The average hourly rate of aggressive acts by the 11 brown booby juniors over the whole trial was more than 7 times greater than that of the 9 blue-footed booby juniors (robust rank order test. 0. Natural broods On two consecutive days.3± 2. then released and observed for three hours between 0800 hours and 1100 hours or 1500 hours and 1800 hours.0–5. with four individuals (in nests B71. at ages 13 days and 15 days. 0.22 aggressive acts per hour compared to 4. performing 34. P<0.

biting and pushing by Brown were first seen at age 17 days. (Drawn by Jaime Zaldivar. Brown attacked Blue continuously whenever Blue was visible nearby (Fig. which is older and 79% heavier. Occasionally Blue responded to aggression with a volley of pecks. initial age/size advantage of nestmate. During the 41 min that both chicks were active that day. Frenzied pecking. 2 Relentless aggression.) neously active. cowered or hid. 3) in response to be- . Relentless aggression was first observed in the four chicks at ages 11–17 days. but also briefly walked out of the nest (Fig. 110 and 711 aggressive acts per hour respectively. compared to maximum rates for the remaining brown booby juniors and the blue-footed booby juniors of 5–54 and 5–41 aggressive acts per hour. but inevitably Brown would renew its assault and Blue would absorb more punishment and adopt submissive postures or flee across the nest. When first observed on day 3. until expulsion of the senior chick in another (described below) and at least 1 day in the last. Brown delivered 224 violent pecks and 8 bites. In nest B71 the blue-footed booby was expelled. when their elder nestmates outweighed them by an average 90%. and in no case was there any indication that aggressiveness was subsiding with time. When attacked on day 5 (22 pecks and 1 bite).D. when Blue was not only obliged on occasions to remain at the nest perimeter exposed to occasional pecks by adult neighbors. 3 A 17-day-old brown booby junior chick expels a blue-footed booby nestmate that is older and 43% heavier. 2). which were paired on day 1 when Brown was 7 days old and Blue was 17. spanning at least 7 days in two individuals. as well as scores of pecks and bites at the attending adult´s tail feathers and wing when Blue was out of sight. although Brown bit Blue 3 times. the 13-day-old brown booby (Sula leucogaster) in nest A55 attacks its blue-footed booby (S. respectively.291 Fig. frequently seizing Blue by the nape or wing and propelling Blue toward the rim of the nest with an expulsion push. 209. On the fifth day of cohabitation. then resumed its frenzied attacking. nebouxii) nestmate. Brown was seldom allowed to even raise its head or beg properly. On four of the next Fig. it received 30 pecks and bites and was frequently forced into submissive and prostrate postures. 1 Aggression (mean±SE) in 11 experimental broods and 9 control broods Fig. Brown attacked incessantly whenever both chicks were active and in proximity. were 282. but its demeanor was sometimes agitated and hurried when being pushed around. There was no evident difference between the four intensely aggressive brown boobies and the other seven brown booby juniors in any independent variable we looked at: age at transfer. except when asleep or under attack. The nature of this intense aggression is illustrated by the interaction in nest A55 of the brown booby junior (“Brown”) and the blue-footed booby senior (“Blue”). Brown briefly became immobile. age at first dominance inversion or latency to first dominance inversion (data not shown). The larger chick flees its own nest to escape frenzied pecking and pushing five observation days (days 7–11). Blue mostly ignored the attacks and continued begging. once even giving a yes-headshake display (Nelson 1978) in brief triumph when Brown crouched down in response. from a photograph by H. it lasted until the end of the trial. Brown prevailed over a much older and larger opponent through aggressiveness and by not being susceptible to intimidation.5 days old. Throughout this period of observations Blue was roughly twice as heavy as Brown. None of the four intensely aggressive chicks died during the study. In every case. When next observed on day 5.

005) and subordinate brown boobies were more than 13 times as aggressive as subordinate blue-footed boobies (robust rank order test.292 ing bitten and pushed (despite weighing 43% more than Brown).10 versus 0.04 pecks. as expected in the blue-footed booby (Fig. 17.51 versus 0.9. Wilcoxon test. P>0. but they responded with submission to similar proportions of pecks (0.20). Dominance inversion by brown booby juniors persisted. n=11. P>0. 8.0. Wilcoxon test. n=11. respectively.15 acts/h.03 pecks) than when it was a bluefooted booby (0.98. only a minority (2 of 7) of surviving bluefoot juniors ever inverted dominance. Indeed. within 2 days a very submissive Blue was spending most of its time 50–70 cm from the nest. after repeated expulsions Blue declined to reenter the nest even when Brown was asleep. Dominance The senior (blue-footed booby) chick was dominant on the first day of behavioral observation in 10 of 11 experimental pairs and in all 9 control pairs. Showing 16 brown booby broods and 17 bluefooted booby broods of the six pairs whose trial continued during several days (1–8 days. T=26.0±0. T=0.1±2. Aggression of seniors Over the whole trial. contrary to our prediction. U=17. Blue approached the nest. respectively.43±0.05. whereas 8 of 10 brown boobies elicited submission from the nestmate (Fisher’s Exact Probability test. Next day. P<0. Senior chicks pecked by juniors were more than twice as likely to respond with a submissive posture when the attacker was a brown booby (0. 4).53. to determine whether the blue-footed booby senior would eventually overcome its smaller assailant.71 acts/h.6 days.1±1. at an age of 15. n=16. P=0.90 versus 3. Mann Whitney test.04±0. 1).02. robust rank order test. X=4.6±0.10±0.3 days) after first inversion.51 days (range=8–21 days). It never did. over at least several days: in each Fig. a majority (11 of 16) of brown booby subordinates pecked or bit. and the two blue-footed boobies did so 3 days and 6 days after transfer. 1). During the brief. n=9. In contrast. while Brown remained in the nest with the attending adult. but the difference was not significant (4. albeit intermittently. Hence. U=0. but as the trials progressed some junior chicks became dominant.015). and if we had not intervened to remove the brown booby. . Natural broods At age 4–9 weeks.71± 0. Fig. 4 Aggression (mean±SE) in natural broods of chicks 4–9 weeks old. This brood was watched for 3 days beyond the period specified by our protocol. P=0.015). there was no clear quantitative difference between them in this respect. at ages 11 days and 17 days. There was an indication that these experimental seniors pitted against brown booby juniors scored higher rates of aggression than control seniors pitted against blue-footed booby juniors.04 pecks.77. the blue-footed booby surely would have died outside the nest. P=0. only 1 of 8 blue-footed booby juniors that pecked aggressively ever provoked a submissive response. Junior chicks of both species commonly responded to pecks by adopting or maintaining a BDFA posture and. P= 0. Persistence after first inversion was less clear for the blue-footed booby juniors: one maintained dominance on 3 of 4 days after first inversion. walked back to the boulder and remained there.20. were no higher than those of their brown booby nestmates (5. The postures of blue-footed booby juniors often looked more stereotyped than those of brown booby juniors. robust rank order test. P=0. dominant brown boobies were more than 7 times as aggressive as dominant blue-footed boobies (robust rank order test. 11. Fig. although high (4. Although when we watched next day Blue was doing all the pecking and Brown was generally submissive. n=8). Fig.51 acts/h. 1).007). n=10. U=2. U=1.0±0. respectively. P=0. the junior chick dominated the senior one on at least half of those days (X=77% of days). but the other one’s trial ended promptly after inversion. respectively. U=1.45±0. whereas only a minority (4 of 17) of blue-footed booby subordinates did so (Fisher’s Exact Probability test. n=9. in experimental broods the aggressive rates of senior chicks. senior chicks in the nine control broods were more than 4 times as aggressive as their junior conspecific nestmates (3. and evidently could have shuffled in and joined its parent.6±0. Brown boobies first inverted dominance 1–15 days after transfer (X=8.035).90 acts/h). a significant difference in proportions (Fisher’s Exact Probability test. P=0. 3-hour observation period. A factor reducing the mean aggressive rates of experimental senior chicks was that four of them spent much of the time cowed by their nestmates’ relentless aggression.0. in the shadow of a boulder. Whereas most (8 of 9) of the surviving brown booby juniors inverted dominance on at least 1 day. but after a pause it turned around.75.04).

but several brown boobies in the 4 to 9-week age range were incidentally seen with a welt and bald patch on the nape where their broodmates were repeatedly seizing. Most subordinate chicks of both species sometimes responded to pecks by adopting a BDFA posture. Two costs of clemency were revealed: a junior chick may sometimes kill the senior chick or.42. Forbes and Ydenberg 1992). and this response appeared more common in subordinate blue footed boobies (0. twisting and thrusting with the mandibles. Brown booby chicks may not be able to physically displace each other at 4–9 weeks in the same way that experimental brown boobies did in the second and third weeks of life. inflicting wounds and defending itself from siblicide (Forbes 1990. were uncontrollably aggressive. In the blue-footed booby. Reported proportions of junior chicks that outsurvive a cohabiting senior broodmate are 3% for the .12 of pecks) than subordinate brown boobies (0. so this requires confirmation. The very early onset of lethal aggression by elder chicks of species that show obligate brood reduction may well be an evolved response to the potential threat posed by their younger broodmates. Only a single push (by a brown booby) was observed in the 34 natural broods of both species. It proposes how two unequal chicks should behave when they inhabit a nest where food will be sufficient to raise only one of them to fledging. and in one case expel it from the nest. in those natural brown booby broods where the junior chick was not promptly killed. We do not know how often and in which circumstances junior chicks kill viable senior chicks. Moreover. P=0.08 of pecks). n=14. aggression from a much larger nestmate. junior brown booby chicks were more aggressive than junior blue-footed booby chicks and some of them.81). the youngest chick is the most belligerent broodmate and comparable to a junior brown booby in its aggressiveness. However. P=0. there was a nonsignificant indication that the summed rate of aggressive acts by the two broodmates declined with increasing age (Spearman’s Correlation. for junior siblings of any avian or mammalian species. resulting in a relationship of fiercely contested dominance that contrasted markedly with the generally stable dominance-subordinance relationships of maturing blue-footed booby broods. Despite having absorbed. their continued nurturance could benefit the inclusive fitness of both elder chick and parents. and might even challenge its broodmate’s aggressive dominance (Forbes and Mock 1996). Mock (personal communication) suggested that in three-chick cattle egret (Bubulcus ibis) broods.293 brown boobies were “subordinate” in the sense of being outpecked. and continuing to absorb. and it is important to be clear about the domain of each. and it is plausible that junior chicks sometimes manage to outcompete and replace viable but inferior senior chicks. U=75.31±0. where the two youngest chicks fight more frequently than any other dyad (Ploger and Mock 1986. Creighton and Schnell 1996). if it manages to survive beyond its roughly 25-day window of vulnerability to permanent eviction. during the following weeks it can impose on the senior chick not just probable foodsharing but also the attrition of fierce aggressive exchanges on a daily basis. the extra chick theoretically can impose increasing costs on its broodmate by competing for food. in the brown booby the high rate of aggressive acts was stable across the age-span sampled (Spearman’s Correlation. Mock and Forbes 1995). it remained highly aggressive during at least the first 7 weeks of life. resource tracking and progeny choice hypotheses (reviews in Forbes 1990.54±0. four of them attacked relentlessly. as far as we know. Discussion As predicted by the desperado sibling hypothesis. RS=–0. 1991.06. and this enabled them to intimidate and subdue the larger chick. it has been recognized that if an extra chick is temporarily allowed to survive in order to extend insurance coverage.19). not in the sense of assuming a nonaggressive role. 15. or eviction may be fruitless at ages when chicks often do not remain on the nest and anyway the victim’s walking ability enables prompt return. because extra chicks are usually handicapped by a substantial age disadvantage and appear to have limited options.09). The laying of extra eggs by brown booby parents is surely explained by some combination of the insurance. but the difference was not significant (Mann Whitney test. Neither empirical nor theoretical studies have analysed the behavioral tactics of extra chicks (but see O’Connor 1978) or contemplated an ability to kill their elder broodmates. P=0. the consequence of this preemptive killing may be that junior chicks are often discarded at a time when. n=16. Likewise. The desperado sibling hypothesis addresses the nature and adaptiveness of chick behavior when parents create a brood that exceeds their capacity to provision (for whatever parental benefit). at least. The field of avian brood reduction and siblicide is abundantly provided with functional hypotheses and models (review in Mock and Parker 1997). if they did not threaten the growth and survival of the elder chick. n=17. Thus. Visible tissue damage through broodmate aggression is rare in blue-footed boobies at any age (personal observation). These experimental and descriptive observations reveal a pattern of aggressiveness not previously reported. RS=0. Field studies of brown boobies (cited in Introduction) show that the extra egg/chick sometimes substitutes for its failed clutchmate/broodmate or even fledges alongside it. youngest cattle egret chicks seldom (Mock and Lamey 1991) or never (Fujioka 1985) initiate fights and their in- dividual pecking frequencies have not been quantified. The demonstration of the fierceness and effectiveness of junior brown boobies in experimental and natural broods confirms and extends the theoretical costs of temporary clemency (sensu Forbes 1990) by elder broodmates and gives an indication of their magnitude. Hitherto. only parental and senior chick perspectives have been examined.

brown boobies can attack any broodmate intensely. but plausibly some senior chick deaths were not due to intrinsic inviability or predation. However. some junior masked boobies (Sula dactylatra) (an obligate brood reducer). Evans and McMahon 1987. Aggressiveness of experimental brown booby chicks varied greatly and it is not clear how much of this variation was due to developmental change. This record suggests that only four out of nine surviving brown booby chicks ever performed relentless aggression and expulsion pushing. It is probable that selection currently favors belligerence (initiating aggression and relentless aggression) of chicks in the junior slot because belligerence occasionally enables them to aggressively substitute their broodmates or fledge alongside them. when given an experimental opportunity to show agonism. The comparative vigor. Ricklefs 1982. given that the junior chicks selected had already managed to survive 7. Timing of agonism may be critical and it is noteworthy that relentless aggression of junior chicks did not begin until several days after the age (7 days) by which most junior chicks in this population have normally fallen victims to siblicide (Tershey et al. our data demonstrate that a brown booby chick can show extreme aggressiveness whether it hatches into the senior slot or the junior slot in the brood.77 days. we should expect to see them routinely killing their sibs before the potential danger of a coup becomes real. 3%. An alternative explanation for the belligerence of some brown booby chicks in the junior slot is that natural selection has had no opportunity to modify aggressive behavior in this context because routine early siblicide means that juniors never get an opportunity to express their aggressiveness.5 days (by which all were dead). but to weak or nonaggressive individuals being overwhelmed by highly aggressive junior siblings. which was frequently used by brown boobies and is rare or nonexistent in blue-footed boobies. Hence. Similarly. We know little about the agonistic strategy of junior brown booby hatchlings and the circumstances in which aggression enables them to prevail. but the question is. No experiments have been performed on any obligate siblicide species to identify variables influencing the aggressiveness of chicks. only that they be able and disposed to do so.294 masked booby (Sula dactylatra. 18% and 6% for the white pelican (Pelecanus erythroryhnchos.0±0. possibly some of the other five junior chicks would eventually have displayed relentless aggression. What passes for insurance benefit may sometimes be aggressive substitution of senior by junior. and 20%. began attacking their broodmates before the juniors reached age 11 days (Anderson 1989). An important function of junior chick aggression could be to resist falling victim to siblicide and fledge alongside the broodmate. the agonism of junior chicks is exposed to natural selection. Such substitution could even benefit parents by improving the quality of their single fledgling. intrinsic differences among individuals or different contingencies in different nests (for example variation among nests in food amount or in behavior of the nestmates or caretaking adults). this hypothesis is not consistent with our observations of some junior chicks surviving alongside their broodmates for several weeks and attacking them strenuously throughout (and see Tershey et al. yielding an incomplete record of aggression over the 24-h period (brown boobies also show broodmate aggression at night. Taken with observations of brown booby senior chicks (Cohen Fernández 1988). Expulsion pushing. Kepler 1969). a 5. Importantly. rather. either by killing their broodmate or by growing up alongside it. Further work on individual variation and on the ontogeny and proximate control of aggression is clearly needed. surely functions to evict and kill the broodmate rather than simply dominate it. and in 1 of the 13 broods observed. aggressiveness and rate of development of hatchling broodmates may greatly influence the outcome of their siblicidal contest (cf. It is tempting to think that individual chicks differ in their intrinsic aggressiveness. it could be argued that there is no specific tendency to attack older and larger broodmates intensely. Cash and Evans 1986.5-day-old junior even expelled its broodmate from the nest for a few minutes. For none of those populations do we have a breakdown of causes of death and the possible role of junior chick aggression. However. if trials had not been suspended when chicks were 18 days old. 2000). This may be so. and that this behavior emerged at age 11–17 days and persisted thereafter. it is not for lack of genetic variation that the brown booby has not done so. 2000). although this ‘progeny choice’ benefit is unlikely to explain laying of the extra egg in a species with just two chicks and a large competitive inequality between them (Forbes and Mock 1998). Werschkul and Jackson 1979. why do brown booby chicks not show the blue-footed booby’s susceptibility to learning subordinance when repeatedly drubbed by a larger and more powerful broodmate? Surely if a congener has evolved the capacity to learn subordination. and that this variation might account for a small minority of nests on San Pedro Mártir actually fledging two chicks (Tershey et al. We critically need to know whether when two chicks fledge. juniors simply expressed the aggressiveness of a senior chick. However. Cohen Fernández 1988). Cohen Fernández (1988) observed aggression in brown booby junior chicks on Isla Isabel before age 6. Bortolotti 1986). In this view. Evans 1996a). Given the large age-based competitive advantage of seniors. A major problem is that our behavioral sampling of individuals was brief (usually 3 h per day). 2000). Certainly our sampling of brown boobies may have favored the inclusion of junior chicks from broods where aggression by the senior chick was relatively mild. the desperado sibling hypothesis does not require that junior chicks frequently kill their broodmates. Contrast of the two species of booby also supports the suggestion that learned losing in the blue-footed booby . the junior one actually recruits into the reproductive population and how much the senior chick’s probability of recruiting diminishes as a consequence of not eliminating its broodmate.

then the susceptibility of bluefooted booby chicks to training in subordinance probably reflects adaptation rather than unavoidable vulnerability of infant birds to violence. in combination with the broodmate’s conditional tolerance. Wilson Bull 99:190–201 Forbes LS (1990) Insurance offspring and the evolution of avian clutch size. Whereas the BDFA posture of the blue-footed booby looks exaggerated as if ritualized for communication. subordinance usually serves their interests better than belligerence (although they sometimes rebel successfully). conspicuous agonistic displays have hitherto been reported only for facultative siblicide species (review in Drummond 2001a). the Mexican Navy for logistical support. If brown booby juniors can sometimes resist being subjugated. Ecology 67:182–194 Cash KJ. Snowdon CT. Brown and blue-footed boobies may lie near the two extremes of a continuum of adaptive variation. but the aggressive and submissive vocal displays reported for 10 facultative siblicide species surely function to communicate with broodmates. García C. vol. Behav Ecol Sociobiol 18:413–418 Castillo A. Gonzalez E. Behav Ecol 12:340–347 Cohen-Fernández EJ (1988) La reducción de la nidada en el bobo café (Sula leucogaster nesiotes Heller and Snodgrass 1901). Canales C (1998) Dominance between booby nestlings involves winner and loser effects. Facultad de Ciencias UNAM Clifford LD. but which evidently leaves the dominant nestmate vulnerable to the assaults of a congeneric desperado. at Ascension. 30. Behav Ecol Sociobiol 19:365–372 Drummond H. en la Isla Isabel. Shelton PC (1976) The natural history of Johnston Atoll. The experiment and observations were authorized by the Secretaría del Medioambiente y Recursos Naturales and carried out in accordance with Mexican law and the ABS/ASAB Guidelines for the Use of Animals in Research. the American white pelican. Blue-footed boobies presumably have evolved the ability to assume a subordinate role because. Central Pacific Ocean. Rosenblatt JS. Evolution 44:2069–2082 Anderson DJ. Undergraduate thesis. Atoll Res Bull 192:213–235 Anderson DJ (1989) The role of hatching asynchrony in siblicidal brood reduction of two booby species. Evans RM (1986) Brood reduction in the American white pelican (Pelecanus erythrorhynchos). blue-footed boobies have evolved a degree of aggressive moderation in the dominant nestmate that allows cohabitation with a subordinate nestmate. Osorno JL (1986) Parent-offspring cooperation in the blue-footed booby (Sula nebouxii): social roles in infanticidal brood reduction. Behav Ecol Sociobiol 25:363–368 Anderson DJ (1990) Evolution of obligate siblicide in boobies. Roper TJ (eds) Advances in the study of the behavior. Ibis 103b:174–220 Drummond H (1993) Have avian parents lost control of offspring aggression? Etología 3:187–198 Drummond H (2001a) The control and function of agonism in avian broodmates. J Theor Biol 147:345–359 Forbes LS (1991) Insurance offspring and brood reduction in a variable environment: the costs and benefits of pessimism. II Food limitation and parent-offspring conflict. Anim Behav 61:1–10 Drummond H. that of the brown booby looks more like an evasive maneuver that simply removes the head from harm’s way. In no species with siblicide have signal functions of supposed agonistic displays been experimentally demonstrated. Jaime Zaldivar for drawing Fig. Regina Macedo. In line with this thinking. Behav Ecol Sociobiol 37:163–168 Bortolotti GR (1986) Evolution of growth rates in eagles: sibling competition vs energy considerations. pp 261–301 Drummond H (2001b) A revaluation of the role of food in nestling aggression. Behav Ecol Sociobiol 39:203–209 Evans RM (1997) Parental investment and quality of insurance offspring in an obligate brood-reducing species. the American white pelican. McMahon BF (1987) Within-brood variation in growth and condition in relation to brood reduction in the American white pelican. Osorno JL. In: Slater PJB. Behav Ecol 8:378–383 Evans RM. Am Nat 138:623–641 Evans RM (1996) Hatching asynchrony and survival of insurance offspring in an obligate brood-reducing species. Doug Mock and José Luis Osorno for comments on the manuscript. Barb Glassey. Merchant H (1991) Sexual dimorphism and sibling competition: implications for avian sex ratios. Anim Behav 55: 1669–1676 Drummond H. and Prescott College for logistical advice and support. Sula nebouxii. Sula spp. Schnell GD (1996) Proximate control of siblicide in cattle egrets: a test of the food amount hypothesis. but absence of ritualization and signal function could account for the general absence of agonistic displays from accounts of obligate siblicide. Oikos 62:325–332 . Scott Forbes.295 is an adaptation. to species whose chicks are implacably aggressive whether they peck or get pecked early in life. Universidad Nacional Autónoma de México Creighton JC. Anderson DJ (2001) Experimental demonstration of the insurance value of extra eggs in an obligately siblicidal seabird. Acknowledgements This research was financed by CONACYT grant 31973 and the UNAM. References Amerson BA. This is a fine and possibly unsustainable distinction. New York. Torres R. Anim Behav 37:806–819 Drummond H. 2. Behav Ecol Sociobiol 38: 371–377 Dorward EF (1962) Comparative biology of the white booby and brown booby. Similarly. Facultad de Ciencias. We are very grateful to Dave Anderson. Bernie Tershey for advice on the logistics and boobies of San Pedro Mártir. Undergraduate thesis. Academic Press. Ricklefs RE (1995) Evidence of kin-selected tolerance by nestlings in a siblicidal bird. Anim Behav 44:881–893 Drummond H. We suspect the brown booby’s BDFA posture may lack a signal function. Nay. This highlights a fundamental assumption of evolutionary stable strategy analyses of conflict: that selection on each role adapts it for dealing specifically with the opposing role(s) it may encounter. Chavez-Peón C (1983) Ecología Reproductiva e influencia del comportamiento en el control del número de crias en el bobo de patas azules. García Chavelas C (1989) Food shortage influences sibling aggresion in the blue-footed booby. from species whose chicks learn early on to be either habitually submissive or habitually aggressive in accordance with their early agonistic experience. 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