Behav Ecol Sociobiol (2003) 53:287–296 DOI 10.1007/s00265-002-0571-2

ORIGINAL ARTICLE

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, Introduction chicks of obligately siblicidal species kill their junior broodmates as early as possible because junior brood- Why do some birds kill their infant siblings as early as mates face dire ecological prospects and are consequently they are apparently able? Among species whose chicks predisposed to aggressively overthrow elder broodmates compete aggressively for dominance and access to pa- by all-out aggression. The agonistic behavior of junior rentally provided food, there is a minority of species that chicks is virtually unknown because they die so young. frequently hatch two chicks, only for one of those chicks We investigated the agonistic behavior of hypothetical routinely to dispatch its broodmate within days of hatch- desperados by fostering junior brown boobies (Sula ing. In this obligate siblicide, the senior (elder) chick re- leucogaster, an obligately siblicidal species) into nests of peatedly pecks, pushes and bites at the broodmate until it the blue-footed booby (S. nebouxii, a facultatively siblic- eventually succumbs through lesions, starvation or ex- idal species) containing an older singleton blue-foot pulsion from the nest (reviews in Mock 1984; Bortolotti chick. Controls were junior blue-footed boobies fostered 1986; Anderson 1990; Mock and Parker 1997). Although into the same situation. Junior brown boobies were in several facultatively siblicidal species aggression of 7 times more aggressive than controls and most of them the elder chick has been shown by experiments to vary dominated their elder and larger nestmates. Four of nine with food deprivation and other factors (reviews in Mock brown booby juniors showed relentless aggression, deliv- and Parker 1997; Drummond 2001a, 2001b), in obligate ering up to 711 pecks, bites and pushes (including “ex- siblicide aggression usually appears urgent and uncondi- pulsion pushes”) per hour, thereby overwhelming nest- tional, and indeed occurs despite apparently adequate mates 90% heavier and permanently expelling one of food provision by parents (e.g., Meyburg 1977; Gargett them from the nest. Similarly, in natural broods of two 1978; Gerhardt et al. 1997). According to the insurance surviving brown booby chicks, the losing chick was hypothesis (Dorward 1962; Mock and Parker 1986; 13 times as aggressive as blue-foot subordinates, up to at Clifford and Anderson 2001), even if parents are incapa- least age 7 weeks. Contrast of the two species of booby ble of provisioning two offspring all the way to indepen- suggests the evolution of agonistic roles within broods dence, they and their senior offspring could often gain in may be partly driven by selection on potential victims to fitness by nurturing or tolerating the junior chick for a express a level and type of aggressiveness appropriate to while lest it be needed to substitute a senior chick that their status-related ecological prospects. proves inviable or suffers predation. Stinson’s (1979) notion of “pending competition” ex- Keywords Aggression · Brood · Desperado · Siblicide · plains why it may be adaptive to dispatch a sibling even Sibling when parental provision is currently sufficient for the two hatchlings: if the developing brood of two will inev- itably outstrip the food supply, then one chick will in the end have to be sacrificed (see also Forbes 1990; Forbes Communicated by C. Brown and Ydenberg 1992). This notion explains the occur- H. Drummond (✉) · C. Rodríguez · A. Vallarino rence and the apparent unconditionality of obligate sibli- C. Valderrábano · G. Rogel · E. Tobón cide, but it does not explain the timing and the urgency. Instituto de Ecología, These features may be explained by the “desperado Universidad Nacional Autónoma de México, A.P. 70–275, 04510 D.F., Mexico sibling” hypothesis (Drummond 1993), derived from e-mail: [email protected] Stinson’s (1979) insight that a junior chick can potential- Tel.: +52-5-6229007, Fax: +52-5-6228997 ly grow to outcompete its initially dominant sibling and 288 Grafen’s (1987) desperado concept. The desperado sib- The agonistic behavior of junior chicks of obligate ling hypothesis applies to species where parents can sel- siblicide species is largely unknown, not only because dom or never provision the whole brood all the way to they spend most of their brief lives concealed under the fledging, and the youngest chick consequently is a desig- parent but also because when visible they are often over- nated victim with near zero prospects of surviving to whelmed by a barrage of attacking and because their breed. In this situation, attempting to overthrow and dis- evasions or struggles command less attention than the place the more powerful competitor is a strategy that car- dramatic violence of their siblings. In facultatively ries negligible cost and should be favored by selection if siblicidal species the agonistic behavior of junior chicks the chick has the physical wherewithal to use violence is somewhat better known (although seldom the focus effectively. In turn, the senior chick, confronted by a of attention), and it varies greatly from conditional ac- competitor disposed to launch an all-out assault, and ceptance of subordination in the blue-footed booby whose relative aggressive prowess increases by the day, (Drummond and Osorno 1992; Drummond and Canales should eliminate the emerging threat as soon as possible. 1998) and western grebe (Aechmophorus occidentalis; Models of siblicide evolution frequently assume that Nuechterlein 1981) to fighting back and even initiating a senior chick has sufficient control to kill its rival at its fighting in great egrets (Casmerodius albus) and brown own convenience (at least when unopposed by parents) pelicans (Pelecanus occidentalis) (review in Drummond and that the junior chick is debarred from killing by 2001a). physical inferiority (e.g. O’Connor 1978; “runt” model To test the desperado sibling hypothesis, we studied in Godfray and Harper 1990). In contrast, the desperado chicks of the brown booby (Sula leucogaster), a ground- sibling hypothesis proposes that siblicide can be an op- nesting species that generally lays one or two eggs and tion for junior chicks, allowing the evolution of brood- often hatches two chicks but rarely raises both of them to mate agonism to be driven partly from below, by selec- independence because the junior one regularly falls vic- tion on the behavior of the designated victim. Conse- tim to broodmate aggression (review in Nelson 1978). quently, the prospect of an attempted coup by the junior The insurance hypothesis seems to account for laying of chick obliges the senior chick to prematurely discard (1) a second egg by this species (Dorward 1962), but excep- the family’s insurance against first chick failure and (2) tionally two chicks may fledge. On Kure Atoll, Johnston whatever (slim) possibility exists of fledging two chicks. Atoll and San Pedro Mártir Island, 16%, 15% and 12% Another hypothesis for the timing of obligate siblici- of second eggs, respectively, provided apparent insur- de holds that parents calibrate the hatching interval (and ance benefit by giving rise to the sole fledgling of the hence the agonistic asymmetry) of their brood so that nest (Woodward 1972; Amerson and Shelton 1976 in killing of the junior chick is guaranteed (Simmons 1988; Nelson 1978; Tershey et al. 2000), although it is not Anderson 1989) and does not occur until after the age clear how much of this benefit accrued through loss of when senior chick survival is assured and insurance is no the senior sibling at the egg versus chick stages. In the longer needed (Evans 1996). Evans’ (1996) observations expanding population of Johnston Atoll, 1.4% of clutch- of an obligately siblicidal population of white pelicans es produced two fledglings each and on San Pedro (Pelecanus erythrorhynchos) showed a high probability Mártir 7% of two-egg clutches that fledged any chicks at of junior chicks surviving through the period when most all fledged two chicks (to the age when they were nearly senior chick deaths occurred (senior ages 0–7 days). fully feathered). The proportion of deaths and age of However, his more detailed observations imply that the mortality in two-chick broods have seldom been quanti- death or lethal debilitation of junior chicks in that popu- fied, but on San Pedro Mártir 65% of junior chicks were lation often occurs when parental interests would require dead within a week, evidently due to injuries, starvation continued survival: half of junior pelican chicks died at and exposure resulting from broodmate attacks and evic- ages 0–6 days, that is, during the period when they could tion (Tershey et al. 2000). Tershey et al. (2000) consid- be called on to provide insurance benefit (Evans 1996), ered that the brown booby on San Pedro Mártir is not and when senior chicks were experimentally removed obligately siblicidal because 7% of two-egg clutches from nests when their junior broodmates were 3 or 6 gave rise to two fledglings, but Simmons (1988) and days old, 21% of those juniors proved to be already too Anderson (1990) considered that siblicide is obligate weakened by sibling harassment and starvation to sur- where fewer than 10% of junior chicks survive. On Isla vive even as singletons (Evans 1997). Evans (1996) cal- Isabel, where brown booby broods were watched 24 h culated that there was a 14% chance that when required per day, all junior chicks that survived predation were to replace a failed a-chick, the b-chick would already be killed within 6.5 days by their broodmates’ round-the- dead. Apparently, valuable insurance is discarded prema- clock pecking, biting and pushing. The senior brown turely. Parents may well adjust the hatching interval to booby chick’s agonistic advantage derives from a large ensure that junior chicks perish at the age when senior initial difference in size and maturity, due to broodmates chicks are safe, and not before. However, parents proba- hatching an average 4.6±0.17 days (mean±SE) apart bly cannot control the behavior of their offspring com- (Cohen Fernández 1988). pletely (Trivers 1974), so intense selection on chicks to We fostered young junior chicks of the brown booby compete for survival could in principle drive the age of into one-chick nests of the facultatively siblicidal blue- death to a lower value than suits parental interests. footed booby, thereby providing each brown booby with 289 an elder nestmate expected to be less aggressive than a nests every 3–7 days, and their ages were estimated from culmen typical brown booby elder broodmate. Provided it is ade- length, using growth curves of blue-footed and brown boobies on Isla Isabel, nearby in the Mexican Pacific Ocean (21º51′N, quately fed, the senior blue-footed booby chick in a two- 105º55′W). Junior brown boobies were scarce, so we used all indi- chick brood usually deploys only enough aggression to viduals aged 2–11 days for which an appropriate experimental ensure the subordination of its broodmate and secure its pairmate could be found, and sought a similar-aged sample of own feeding priority (Drummond and García Chavelas blue-footed booby juniors for the control treatment. Although the identification of junior chicks was certain, because each one was 1989; Anderson and Ricklefs 1995). The senior blue- found cohabiting with a larger broodmate, it is likely that a minor- footed booby chick is 4.0±0.36 days older than its brood- ity of the singleton blue-footed booby chicks were survivors of mate (Castillo and Chavez-Peón 1983). After some early two-chick broods reduced by junior chick death (or even senior beatings, the junior blue-footed booby broodmate largely chick death), but this probability was the same for experimental renounces its attempts at aggression and routinely and control pairs. Sex of chicks was not known. The experimental subjects were 11 brown booby junior chicks concedes to attacks and aggressive displays by adopting of age 7.0±0.77 days and weighing 104±12.7 g, which were trans- the submissive bill-down-and-face-away posture (BDFA; ferred into blue-footed booby nests containing singleton chicks of Nelson 1978). By this time, the senior chick is a age 12.4±1.15 days and weighing 198±24.9 g, yielding 11 pairs in ‘trained winner’ and the junior chick is a ‘trained loser’ which the senior chick was 5.5±0.84 days older and initially 91±12.1% heavier than its nestmate. The control subjects were (Drummond and Osorno 1992; Drummond and Canales nine blue-footed booby junior chicks of age 7.3±1.18 days and 1998). The senior chick allows the junior chick to cohab- weighing 97±16.1 g, which were transferred into blue-footed boo- it and share resources for several days or weeks, often by nests containing singleton chicks of age 13.2±1.27 days and until both birds become independent at about 4 months weighing 209±33.3 g, yielding nine pairs in which the senior chick was 5.8±0.87 days older and 117±21.7% heavier than the of age. Junior blue-footed boobies can become aggres- resident chick. Hence, in both samples the average age difference sive if they detect weakness in their broodmate, but they between nestmates was slightly greater than the average difference seldom manage to invert the dominance relationship (ex- in natural broods of the junior chick’s own species. ample in Drummond et al. 1991). Trials ended when the junior chick reached age 18 days, after We reasoned that a junior brown booby chick would an average 11 days cohabitation in the foster nest, except for the four trials (two in each treatment) where the junior chick died ear- probably survive longer in the nest of its congener, al- lier. Experimental and control trials ran during roughly the same lowing us to describe the agonistic behavior of a young dates. Setting the date the first trial started as 1, start dates of brown booby chick confronted by a larger, older and experimental trials and control trials were 3.4±0.88 and 3.4±1.03, more powerful competitor. Trials ended when we trans- respectively. Experimental trials ended when we permanently transferred the brown booby junior to a conspecific nest contain- ferred the brown boobies back into a conspecific nest ing a similar-sized chick. We observed these nests for several days while they were still young enough to integrate into the and confirmed that the foster chicks were accepted by the adults. family. For the control treatment, we fostered young ju- Control trials ended when we suspended observation of the two nior blue-footed boobies into conspecific nests contain- nestmates, simply leaving the junior chick in its foster nest (to save it the challenge of reintegrating into the home nest). ing a single older chick. The desperado sibling hypothe- Each trial started when the junior chick was removed from its sis predicts that in comparison with controls, brown boo- home nest, wrapped in cloth and transported (in less than 20 min) by juniors should be uncontrollable: highly aggressive to the foster nest. There, the resident chick was removed, both except when overwhelmed, and non-submissive beyond chicks were weighed with a spring balance, measured (culmen), temporary evasion and avoidance (Drummond 2001a). fitted with a numbered plastic leg band and marked on the head and rump with red, yellow or blue acrylic paint (colors assigned Additionally, we took advantage of the existence of haphazardly) for identification during observations. Then both natural surviving pairs of brown booby broodmates in chicks were inserted simultaneously into the center of the nest and the 2001 season, to make a comparison of agonism in the “family” was watched to confirm acceptance of the chicks, maturing brown booby broods versus maturing blue- which always occurred. Observers watched one pair, exceptionally two pairs, at a footed booby broods. In blue-footed booby broods de- time, alternating whenever possible between morning (0800– scribed by Drummond et al. (1986), aggression peaked at 1100 hours) and afternoon observations (1500–1800 hours) of ages 10–20 days, then declined more or less progressive- each pair. Each pair was watched every day for 3 h, except on ex- ly between ages 3 to 9 weeks. The desperado sibling ceptional days when insufficient observers were available, when observation was suspended or reduced to 1.5 h. Observation start- hypothesis predicts that in maturing two-chick broods of ed the day after transfer, although the youngest juniors were not the brown booby aggression by both broodmates should observed until the second or third day after transfer (very young be more intense and decline less with age than in the chicks are brooded and can seldom be seen). The 11 experimental blue-footed booby, as nestmates continue striving to pairs were observed on 7.9±1.02 days, starting when the junior eliminate each other rather than adopting a relationship chick was 8.4±0.65 days old, and the 9 control pairs were ob- served on 7.9±0.34 days, starting when the junior chick was of dominance-subordination. 8.6±1.10 days old. At the end of each day’s observation, the chicks were weighed and measured, and their paint marks were renewed if necessary. Methods The observer sat 4–6 m from the focal nest without a blind (boobies with chicks are extraordinarily tolerant of human pres- Fostering experiment ence), and recorded the absolute frequency of pecks (impact of the bill on the victim), bites (the victim is seized in the mandibles for The experiment was carried out in March 2001 on the island of at least 1 s), pushes (the seized victim is displaced at least 1 cm by San Pedro Mártir, in the Sea of Cortéz (28º23′N, 112º20′W). thrusting with the mandibles), and expulsions (the victim is forced Chicks were selected for the experiment by surveying about 1,000 or flees across the perimeter rim of the nest), noting also for each 290 peck whether the victim was submissive (adopted or sustained a boobies were similar to those of same-aged conspecific BDFA posture). The observer also recorded every half minute singletons (including senior chicks whose broodmates (signaled precisely by a bleep) whether each chick was inactive (head resting on any substrate or invisible under attending adult) had died) on Isla Isabel, Nayarít, and weights of the ju- or active in that instant. This last record was taken in order to de- nior blue-footed boobies were similar to those of same- termine how much of the time both pairmates were simultaneously aged junior conspecifics on Isla Isabel (data not shown). awake and therefore available to interact (chicks sleep most of the Hence, it seems that the brown booby chicks were ade- time) and discriminate whether different frequencies of aggression were due to aggressiveness versus opportunity to attack. quately cared for by blue-footed booby adults. For analysis, attacks, bites and pushes were summed together Aggression was mostly pecking, followed in frequen- as aggressive acts, and a chick was considered dominant on any cy by biting and then pushing. Across the whole trial, the particular day if it performed more aggressive acts than its nest- following average proportions of those acts, respectively, mate. All statistical tests were two-tailed and we compared medi- were performed by brown booby juniors (0.501, 0.466, an aggressive rates in independent samples with the robust rank order test (Hollander and Wolfe 1999) when unequal variances 0.032), their nestmates (0.755, 0.230, 0.015), blue-footed precluded use of the Mann-Whitney U-test (Kasuya 2001). Sam- booby juniors (0.459, 0.427, 0.013) and their nestmates ple values are expressed as mean±SE throughout. (0.689, 0.204, 0.008). However, only the brown booby performed “expulsion pushing”, systematically grasping Natural broods the rival’s body part (often the nape or wing) in its man- dibles for several seconds while thrusting forcefully out- On two consecutive days, each of five observers searched the colo- ward and upward and, if possible, walking forward. Re- ny for broods of two chicks more than 4 weeks old, selecting the corded as a bite or push, this behavioral pattern func- first observable brood or pair of broods encountered (later we dis- carded a few broods to make the samples of both species similar in tioned to displace the rival, sometimes as far as several age). Chicks were captured by hand, measured (culmen) to estimate bodylengths and, together with more horizontal pushing age and paint-marked for individual identification, then released and with open or closed mandibles, was the brown booby’s observed for three hours between 0800 hours and 1100 hours or main mechanism for evicting a broodmate. 1500 hours and 1800 hours, using the same behavioral recording Brown booby juniors were individually active during system used in the experiment. We could not reliably determine which broodmate was the elder since at these ages the larger body an average 22% of the observation time and simulta- size of females confuses comparisons of unsexed birds. So, instead neously active with their pairmates during 14% of the of sorting data by junior versus senior chick we sorted by dominant time, and for blue-footed booby juniors the average per- versus subordinate chick, according to which broodmate performed centages were similar (23% and 15%, respectively). more aggressive acts (we did not take submissive behavior into ac- count). The samples obtained were 16 brown booby broods, with Hence, rates of aggression are simply expressed per hour subordinate chicks 29–51 days old (40.2±1.67 days) and 17 blue- of observation except where otherwise noted. footed booby broods with subordinate chicks 28–59 days old (43.3±2.24 days); the 16 dominant brown boobies were 30–60 days old (42.9±2.19 days) and the 17 dominant blue-footed boobies were 30–64 days old (46.3± 2.43 days). Aggression of juniors The average hourly rate of aggressive acts by the 11 Results brown booby juniors over the whole trial was more than 7 times greater than that of the 9 blue-footed booby ju- Fostering experiment niors (robust rank order test, U=−2.39, P<0.05; Fig. 1). A similar difference was observed in rates of aggressive General acts during times when both nestmates were simulta- neously active: brown booby juniors were eight times as The junior chick died before the end of the trial in 2 of 11 aggressive as blue-footed booby juniors, performing 34.4 experimental pairs, at ages 13 days and 15 days, and in 2 ± 21.22 aggressive acts per hour compared to 4.3±1.01 of 9 control pairs, at ages 12 days and 15 days. One of acts per hour (robust rank order test, U=−3.07, P<0.025). these brown booby juniors steadily lost weight over Among the brown booby juniors, individual variation 5 days and was found dead on the nest, the other gained in aggressiveness was great, with four individuals (in weight normally and was found dead 15 cm from the nest. nests B71, B57, B78 and A55) forming a distinct sub- The two blue-footed booby juniors disappeared from the group marked by long bouts of attacking that was relent- nest; one had been growing normally and the other had less in the sense that as long as both chicks were awake gained no weight in the last 3 days. The four deaths were and the senior one was visible and within striking dis- similar to typical junior chick losses in the blue-footed tance, the junior chick never ceased attacking unless it booby and probably associated with junior status. No ex- was itself attacked. The maximum rates of aggression ceptional behavior was observed in any of the four broods. scored by these four individuals on any day were 64, 45, All senior chicks remained larger than their foster 31 and 81 aggressive acts per hour, respectively, consid- nestmates throughout the trials, and on the last day of erably greater than the maximum values for the remain- observation the experimental and control seniors in pairs ing seven brown booby juniors and the nine blue-footed that suffered no mortality were 53±11.6% (n=9) and booby juniors of 0.3–6.9 and 1.0–5.0 aggressive acts per 85±25.2% (n=7) larger than their junior nestmates, re- hour, respectively. The maximum daily rates of the four spectively. At that time, weights of the junior brown individuals, at times when both nestmates were simulta- 291

Fig. 2 Relentless aggression. On the fifth day of cohabitation, the 13-day-old brown booby (Sula leucogaster) in nest A55 attacks its Fig. 1 Aggression (mean±SE) in 11 experimental broods and 9 blue-footed booby (S. nebouxii) nestmate, which is older and 79% control broods heavier. (Drawn by Jaime Zaldivar, from a photograph by H.D.) neously active, were 282, 209, 110 and 711 aggressive acts per hour respectively, compared to maximum rates for the remaining brown booby juniors and the blue-foot- ed booby juniors of 5–54 and 5–41 aggressive acts per hour, respectively. Relentless aggression was first ob- served in the four chicks at ages 11–17 days, when their elder nestmates outweighed them by an average 90%. In every case, it lasted until the end of the trial, spanning at least 7 days in two individuals, until expulsion of the se- nior chick in another (described below) and at least 1 day in the last, and in no case was there any indication that aggressiveness was subsiding with time. There was no evident difference between the four intensely aggres- sive brown boobies and the other seven brown booby ju- niors in any independent variable we looked at: age at transfer, initial age/size advantage of nestmate, age at Fig. 3 A 17-day-old brown booby junior chick expels a blue-foot- first dominance inversion or latency to first dominance ed booby nestmate that is older and 43% heavier. The larger chick inversion (data not shown). None of the four intensely flees its own nest to escape frenzied pecking and pushing aggressive chicks died during the study. The nature of this intense aggression is illustrated by five observation days (days 7–11), Brown attacked inces- the interaction in nest A55 of the brown booby junior santly whenever both chicks were active and in proximi- (“Brown”) and the blue-footed booby senior (“Blue”), ty, frequently seizing Blue by the nape or wing and pro- which were paired on day 1 when Brown was 7 days old pelling Blue toward the rim of the nest with an expulsion and Blue was 17.5 days old. When first observed on day push. Blue mostly ignored the attacks and continued beg- 3, although Brown bit Blue 3 times, it received 30 pecks ging, but its demeanor was sometimes agitated and hur- and bites and was frequently forced into submissive and ried when being pushed around. Occasionally Blue re- prostrate postures; Brown was seldom allowed to even sponded to aggression with a volley of pecks, once even raise its head or beg properly. When next observed on giving a yes-headshake display (Nelson 1978) in brief tri- day 5, except when asleep or under attack, Brown at- umph when Brown crouched down in response, but inevi- tacked Blue continuously whenever Blue was visible tably Brown would renew its assault and Blue would ab- nearby (Fig. 2). During the 41 min that both chicks were sorb more punishment and adopt submissive postures or active that day, Brown delivered 224 violent pecks and 8 flee across the nest. Throughout this period of observa- bites, as well as scores of pecks and bites at the attending tions Blue was roughly twice as heavy as Brown. adult´s tail feathers and wing when Blue was out of sight. In nest B71 the blue-footed booby was expelled. Brown prevailed over a much older and larger opponent Frenzied pecking, biting and pushing by Brown were through aggressiveness and by not being susceptible to first seen at age 17 days, when Blue was not only intimidation. When attacked on day 5 (22 pecks and 1 obliged on occasions to remain at the nest perimeter ex- bite), Brown briefly became immobile, cowered or hid, posed to occasional pecks by adult neighbors, but also then resumed its frenzied attacking. On four of the next briefly walked out of the nest (Fig. 3) in response to be- 292 ing bitten and pushed (despite weighing 43% more than Brown). Although when we watched next day Blue was doing all the pecking and Brown was generally submis- sive, within 2 days a very submissive Blue was spending most of its time 50–70 cm from the nest, in the shadow of a boulder, while Brown remained in the nest with the attending adult. Next day, after repeated expulsions Blue declined to reenter the nest even when Brown was asleep. Blue approached the nest, and evidently could have shuffled in and joined its parent, but after a pause it turned around, walked back to the boulder and remained there. This brood was watched for 3 days beyond the pe- riod specified by our protocol, to determine whether the blue-footed booby senior would eventually overcome its smaller assailant. It never did, and if we had not inter- vened to remove the brown booby, the blue-footed boo- Fig. 4 Aggression (mean±SE) in natural broods of chicks by surely would have died outside the nest. 4–9 weeks old. Showing 16 brown booby broods and 17 blue- footed booby broods Aggression of seniors of the six pairs whose trial continued during several days Over the whole trial, senior chicks in the nine control (1–8 days, X=4.3 days) after first inversion, the junior broods were more than 4 times as aggressive as their chick dominated the senior one on at least half of those junior conspecific nestmates (3.0±0.51 versus 0.71± days (X=77% of days). Persistence after first inversion 0.15 acts/h, respectively; Wilcoxon test, T=0.0, n=9, was less clear for the blue-footed booby juniors: one P=0.007), as expected in the blue-footed booby (Fig. 1). maintained dominance on 3 of 4 days after first inversion, In contrast, in experimental broods the aggressive rates of but the other one’s trial ended promptly after inversion. senior chicks, although high (4.6±0.90 acts/h), were no Junior chicks of both species commonly responded to higher than those of their brown booby nestmates pecks by adopting or maintaining a BDFA posture and, (5.1±2.71 acts/h; Wilcoxon test, T=26.0, n=11, P= 0.53; contrary to our prediction, there was no clear quantita- Fig. 1). There was an indication that these experimental tive difference between them in this respect. The pos- seniors pitted against brown booby juniors scored higher tures of blue-footed booby juniors often looked more ste- rates of aggression than control seniors pitted against reotyped than those of brown booby juniors, but they re- blue-footed booby juniors, but the difference was not sig- sponded with submission to similar proportions of pecks nificant (4.6±0.90 versus 3.0±0.51 acts/h, respectively; (0.45±0.10 versus 0.43±0.04 pecks, respectively; robust robust rank order test, U=1.02, n=11,9, P>0.20; Fig. 1). A rank order test, U=0.75, n=9, 11, P>0.20). Senior chicks factor reducing the mean aggressive rates of experimental pecked by juniors were more than twice as likely to re- senior chicks was that four of them spent much of the spond with a submissive posture when the attacker was a time cowed by their nestmates’ relentless aggression. brown booby (0.10±0.03 pecks) than when it was a blue- footed booby (0.04±0.04 pecks; Mann Whitney test, U=17, n=10, 8, P=0.04). Indeed, only 1 of 8 blue-footed Dominance booby juniors that pecked aggressively ever provoked a submissive response, whereas 8 of 10 brown boobies The senior (blue-footed booby) chick was dominant on elicited submission from the nestmate (Fisher’s Exact the first day of behavioral observation in 10 of 11 experi- Probability test, P=0.015). mental pairs and in all 9 control pairs, but as the trials progressed some junior chicks became dominant. Whereas most (8 of 9) of the surviving brown booby ju- Natural broods niors inverted dominance on at least 1 day, only a minor- ity (2 of 7) of surviving bluefoot juniors ever inverted At age 4–9 weeks, dominant brown boobies were more dominance, a significant difference in proportions than 7 times as aggressive as dominant blue-footed boo- (Fisher’s Exact Probability test, P=0.035). Brown boo- bies (robust rank order test, n=16, 17, U=2.77, P=0.005) bies first inverted dominance 1–15 days after tran- and subordinate brown boobies were more than 13 times sfer (X=8.6 days, n=8), at an age of 15.1±1.51 days as aggressive as subordinate blue-footed boobies (robust (range=8–21 days), and the two blue-footed boobies did rank order test, U=1.98, P<0.05; Fig. 4). During the so 3 days and 6 days after transfer, at ages 11 days and brief, 3-hour observation period, a majority (11 of 16) of 17 days, respectively. brown booby subordinates pecked or bit, whereas only a Dominance inversion by brown booby juniors persist- minority (4 of 17) of blue-footed booby subordinates did ed, albeit intermittently, over at least several days: in each so (Fisher’s Exact Probability test, P=0.015). Hence, 293 brown boobies were “subordinate” in the sense of being dividual pecking frequencies have not been quantified, outpecked, not in the sense of assuming a nonaggressive so this requires confirmation. role. In the blue-footed booby, there was a nonsignificant The field of avian brood reduction and siblicide is indication that the summed rate of aggressive acts by the abundantly provided with functional hypotheses and two broodmates declined with increasing age (Spear- models (review in Mock and Parker 1997), and it is im- man’s Correlation, RS=–0.42, n=17, P=0.09); in the portant to be clear about the domain of each. The laying brown booby the high rate of aggressive acts was stable of extra eggs by brown booby parents is surely explained across the age-span sampled (Spearman’s Correlation, by some combination of the insurance, resource tracking RS=0.06, n=16, P=0.81). Most subordinate chicks of and progeny choice hypotheses (reviews in Forbes 1990, both species sometimes responded to pecks by adopting 1991; Mock and Forbes 1995). Field studies of brown a BDFA posture, and this response appeared more com- boobies (cited in Introduction) show that the extra mon in subordinate blue footed boobies (0.54±0.12 of egg/chick sometimes substitutes for its failed clutch- pecks) than subordinate brown boobies (0.31±0.08 of mate/broodmate or even fledges alongside it, and it is pecks), but the difference was not significant (Mann plausible that junior chicks sometimes manage to out- Whitney test, n=14, 15, U=75, P=0.19). compete and replace viable but inferior senior chicks. Visible tissue damage through broodmate aggression The desperado sibling hypothesis addresses the nature is rare in blue-footed boobies at any age (personal obser- and adaptiveness of chick behavior when parents create a vation), but several brown boobies in the 4 to 9-week brood that exceeds their capacity to provision (for what- age range were incidentally seen with a welt and bald ever parental benefit). It proposes how two unequal patch on the nape where their broodmates were repeated- chicks should behave when they inhabit a nest where ly seizing, twisting and thrusting with the mandibles. food will be sufficient to raise only one of them to fledg- Only a single push (by a brown booby) was observed in ing. Hitherto, it has been recognized that if an extra the 34 natural broods of both species. Brown booby chick is temporarily allowed to survive in order to ex- chicks may not be able to physically displace each other tend insurance coverage, the extra chick theoretically can at 4–9 weeks in the same way that experimental brown impose increasing costs on its broodmate by competing boobies did in the second and third weeks of life, or for food, inflicting wounds and defending itself from sib- eviction may be fruitless at ages when chicks often do licide (Forbes 1990; Forbes and Ydenberg 1992), and not remain on the nest and anyway the victim’s walking might even challenge its broodmate’s aggressive domi- ability enables prompt return. nance (Forbes and Mock 1996). Neither empirical nor theoretical studies have analysed the behavioral tactics of extra chicks (but see O’Connor 1978) or contemplated Discussion an ability to kill their elder broodmates, because extra chicks are usually handicapped by a substantial age dis- As predicted by the desperado sibling hypothesis, junior advantage and appear to have limited options. Thus, only brown booby chicks were more aggressive than junior parental and senior chick perspectives have been exam- blue-footed booby chicks and some of them, at least, ined. The demonstration of the fierceness and effective- were uncontrollably aggressive. Despite having ab- ness of junior brown boobies in experimental and natural sorbed, and continuing to absorb, aggression from a broods confirms and extends the theoretical costs of tem- much larger nestmate, four of them attacked relentlessly, porary clemency (sensu Forbes 1990) by elder brood- and this enabled them to intimidate and subdue the larger mates and gives an indication of their magnitude. The chick, and in one case expel it from the nest. Likewise, very early onset of lethal aggression by elder chicks of in those natural brown booby broods where the junior species that show obligate brood reduction may well be chick was not promptly killed, it remained highly ag- an evolved response to the potential threat posed by their gressive during at least the first 7 weeks of life, resulting younger broodmates. Moreover, the consequence of this in a relationship of fiercely contested dominance that preemptive killing may be that junior chicks are often contrasted markedly with the generally stable domi- discarded at a time when, if they did not threaten the nance-subordinance relationships of maturing blue-foot- growth and survival of the elder chick, their continued ed booby broods. These experimental and descriptive ob- nurturance could benefit the inclusive fitness of both el- servations reveal a pattern of aggressiveness not previ- der chick and parents. ously reported, as far as we know, for junior siblings of Two costs of clemency were revealed: a junior chick any avian or mammalian species. Mock (personal com- may sometimes kill the senior chick or, if it manages to munication) suggested that in three-chick cattle egret survive beyond its roughly 25-day window of vulnerabil- (Bubulcus ibis) broods, where the two youngest chicks ity to permanent eviction, during the following weeks it fight more frequently than any other dyad (Ploger and can impose on the senior chick not just probable food- Mock 1986; Creighton and Schnell 1996), the youngest sharing but also the attrition of fierce aggressive ex- chick is the most belligerent broodmate and comparable changes on a daily basis. We do not know how often and to a junior brown booby in its aggressiveness. However, in which circumstances junior chicks kill viable senior youngest cattle egret chicks seldom (Mock and Lamey chicks. Reported proportions of junior chicks that out- 1991) or never (Fujioka 1985) initiate fights and their in- survive a cohabiting senior broodmate are 3% for the 294 masked booby (Sula dactylatra; Kepler 1969), and 20%, aggression enables them to prevail, either by killing their 3%, 18% and 6% for the white pelican (Pelecanus broodmate or by growing up alongside it. Expulsion erythroryhnchos; Cash and Evans 1986; Evans and pushing, which was frequently used by brown boobies McMahon 1987; Evans 1996a). For none of those popu- and is rare or nonexistent in blue-footed boobies, surely lations do we have a breakdown of causes of death and functions to evict and kill the broodmate rather than sim- the possible role of junior chick aggression, but plausibly ply dominate it. Timing of agonism may be critical and it some senior chick deaths were not due to intrinsic invia- is noteworthy that relentless aggression of junior chicks bility or predation, but to weak or nonaggressive individ- did not begin until several days after the age (7 days) by uals being overwhelmed by highly aggressive junior sib- which most junior chicks in this population have normal- lings. What passes for insurance benefit may sometimes ly fallen victims to siblicide (Tershey et al. 2000). How- be aggressive substitution of senior by junior. Such sub- ever, Cohen Fernández (1988) observed aggression in stitution could even benefit parents by improving the brown booby junior chicks on Isla Isabel before age quality of their single fledgling, although this ‘progeny 6.5 days (by which all were dead), and in 1 of the 13 choice’ benefit is unlikely to explain laying of the extra broods observed, a 5.5-day-old junior even expelled its egg in a species with just two chicks and a large compet- broodmate from the nest for a few minutes. Similarly, itive inequality between them (Forbes and Mock 1998). some junior masked boobies (Sula dactylatra) (an obli- The comparative vigor, aggressiveness and rate of devel- gate brood reducer), began attacking their broodmates opment of hatchling broodmates may greatly influence before the juniors reached age 11 days (Anderson 1989). the outcome of their siblicidal contest (cf. Werschkul and An important function of junior chick aggression could Jackson 1979; Ricklefs 1982; Bortolotti 1986). Impor- be to resist falling victim to siblicide and fledge along- tantly, the desperado sibling hypothesis does not require side the broodmate. We critically need to know whether that junior chicks frequently kill their broodmates, only when two chicks fledge, the junior one actually recruits that they be able and disposed to do so. Given the large into the reproductive population and how much the se- age-based competitive advantage of seniors, we should nior chick’s probability of recruiting diminishes as a expect to see them routinely killing their sibs before the consequence of not eliminating its broodmate. potential danger of a coup becomes real. Taken with observations of brown booby senior Aggressiveness of experimental brown booby chicks chicks (Cohen Fernández 1988), our data demonstrate varied greatly and it is not clear how much of this varia- that a brown booby chick can show extreme aggressive- tion was due to developmental change, intrinsic differ- ness whether it hatches into the senior slot or the junior ences among individuals or different contingencies in slot in the brood. Hence, it could be argued that there is different nests (for example variation among nests in no specific tendency to attack older and larger brood- food amount or in behavior of the nestmates or caretak- mates intensely; rather, brown boobies can attack any ing adults). A major problem is that our behavioral sam- broodmate intensely. This may be so, but the question is, pling of individuals was brief (usually 3 h per day), why do brown booby chicks not show the blue-footed yielding an incomplete record of aggression over the booby’s susceptibility to learning subordinance when re- 24-h period (brown boobies also show broodmate ag- peatedly drubbed by a larger and more powerful brood- gression at night; Cohen Fernández 1988). This record mate? Surely if a congener has evolved the capacity to suggests that only four out of nine surviving brown boo- learn subordination, it is not for lack of genetic variation by chicks ever performed relentless aggression and ex- that the brown booby has not done so. It is probable that pulsion pushing, and that this behavior emerged at age selection currently favors belligerence (initiating aggres- 11–17 days and persisted thereafter. However, if trials sion and relentless aggression) of chicks in the junior had not been suspended when chicks were 18 days old, slot because belligerence occasionally enables them to possibly some of the other five junior chicks would aggressively substitute their broodmates or fledge along- eventually have displayed relentless aggression. No ex- side them. periments have been performed on any obligate siblicide An alternative explanation for the belligerence of species to identify variables influencing the aggressive- some brown booby chicks in the junior slot is that natu- ness of chicks. It is tempting to think that individual ral selection has had no opportunity to modify aggres- chicks differ in their intrinsic aggressiveness, and that sive behavior in this context because routine early sibli- this variation might account for a small minority of cide means that juniors never get an opportunity to ex- nests on San Pedro Mártir actually fledging two chicks press their aggressiveness. In this view, when given an (Tershey et al. 2000). Certainly our sampling of brown experimental opportunity to show agonism, juniors sim- boobies may have favored the inclusion of junior chicks ply expressed the aggressiveness of a senior chick. How- from broods where aggression by the senior chick was ever, this hypothesis is not consistent with our observa- relatively mild, given that the junior chicks selected had tions of some junior chicks surviving alongside their already managed to survive 7.0±0.77 days. Further work broodmates for several weeks and attacking them strenu- on individual variation and on the ontogeny and proxi- ously throughout (and see Tershey et al. 2000); the agon- mate control of aggression is clearly needed. ism of junior chicks is exposed to natural selection. We know little about the agonistic strategy of junior Contrast of the two species of booby also supports the brown booby hatchlings and the circumstances in which suggestion that learned losing in the blue-footed booby 295 is an adaptation. If brown booby juniors can sometimes References resist being subjugated, then the susceptibility of blue- footed booby chicks to training in subordinance probably Amerson BA, Shelton PC (1976) The natural history of Johnston reflects adaptation rather than unavoidable vulnerability Atoll, Central Pacific Ocean. Atoll Res Bull 192:213–235 Anderson DJ (1989) The role of hatching asynchrony in siblicidal of infant birds to violence. Blue-footed boobies presum- brood reduction of two booby species. Behav Ecol Sociobiol ably have evolved the ability to assume a subordinate 25:363–368 role because, in combination with the broodmate’s con- Anderson DJ (1990) Evolution of obligate siblicide in boobies. ditional tolerance, subordinance usually serves their in- II Food limitation and parent-offspring conflict. Evolution 44:2069–2082 terests better than belligerence (although they sometimes Anderson DJ, Ricklefs RE (1995) Evidence of kin-selected toler- rebel successfully). Similarly, blue-footed boobies have ance by nestlings in a siblicidal bird. Behav Ecol Sociobiol evolved a degree of aggressive moderation in the domi- 37:163–168 nant nestmate that allows cohabitation with a subordi- Bortolotti GR (1986) Evolution of growth rates in eagles: sibling nate nestmate, but which evidently leaves the dominant competition vs energy considerations. Ecology 67:182–194 Cash KJ, Evans RM (1986) Brood reduction in the American nestmate vulnerable to the assaults of a congeneric des- white pelican (Pelecanus erythrorhynchos). Behav Ecol Socio- perado. This highlights a fundamental assumption of biol 18:413–418 evolutionary stable strategy analyses of conflict: that se- Castillo A, Chavez-Peón C (1983) Ecología Reproductiva e in- lection on each role adapts it for dealing specifically fluencia del comportamiento en el control del número de crias en el bobo de patas azules, Sula nebouxii, en la Isla Isabel, with the opposing role(s) it may encounter. Brown and Nay. Undergraduate thesis, Facultad de Ciencias UNAM blue-footed boobies may lie near the two extremes of a Clifford LD, Anderson DJ (2001) Experimental demonstration of continuum of adaptive variation, from species whose the insurance value of extra eggs in an obligately siblicidal chicks learn early on to be either habitually submissive seabird. Behav Ecol 12:340–347 Cohen-Fernández EJ (1988) La reducción de la nidada en el bobo or habitually aggressive in accordance with their early café (Sula leucogaster nesiotes Heller and Snodgrass 1901). agonistic experience, to species whose chicks are impla- Undergraduate thesis, Facultad de Ciencias, Universidad cably aggressive whether they peck or get pecked early Nacional Autónoma de México in life. Creighton JC, Schnell GD (1996) Proximate control of siblicide in Adoption of the BDFA posture by junior brown boo- cattle egrets: a test of the food amount hypothesis. Behav Ecol Sociobiol 38: 371–377 bies was surprising because the desperado sibling hy- Dorward EF (1962) Comparative biology of the white booby and pothesis predicts that in an obligate siblicide species ju- brown booby, Sula spp. at Ascension. Ibis 103b:174–220 nior chicks will not signal submission and senior chicks Drummond H (1993) Have avian parents lost control of offspring will not moderate their aggression in response to submis- aggression? Etología 3:187–198 Drummond H (2001a) The control and function of agonism in avi- sion. In line with this thinking, conspicuous agonistic an broodmates. In: Slater PJB, Rosenblatt JS, Snowdon CT, displays have hitherto been reported only for facultative Roper TJ (eds) Advances in the study of the behavior, vol. 30. siblicide species (review in Drummond 2001a). In no Academic Press, New York, pp 261–301 species with siblicide have signal functions of supposed Drummond H (2001b) A revaluation of the role of food in nestling aggression. Anim Behav 61:1–10 agonistic displays been experimentally demonstrated, but Drummond H, Canales C (1998) Dominance between booby the aggressive and submissive vocal displays reported nestlings involves winner and loser effects. Anim Behav 55: for 10 facultative siblicide species surely function to 1669–1676 communicate with broodmates. We suspect the brown Drummond H, García Chavelas C (1989) Food shortage influenc- booby’s BDFA posture may lack a signal function. es sibling aggresion in the blue-footed booby. Anim Behav 37:806–819 Whereas the BDFA posture of the blue-footed booby Drummond H, Osorno JL (1992) Training siblings to be submis- looks exaggerated as if ritualized for communication, sive losers: dominance between booby nestlings. Anim Behav that of the brown booby looks more like an evasive ma- 44:881–893 neuver that simply removes the head from harm’s way. Drummond H, Gonzalez E, Osorno JL (1986) Parent-offspring co- operation in the blue-footed booby (Sula nebouxii): social This is a fine and possibly unsustainable distinction, but roles in infanticidal brood reduction. Behav Ecol Sociobiol absence of ritualization and signal function could ac- 19:365–372 count for the general absence of agonistic displays from Drummond H, Osorno JL, García C, Torres R, Merchant H (1991) accounts of obligate siblicide. Sexual dimorphism and sibling competition: implications for avian sex ratios. Am Nat 138:623–641 Evans RM (1996) Hatching asynchrony and survival of insurance Acknowledgements This research was financed by CONACYT offspring in an obligate brood-reducing species, the American grant 31973 and the UNAM. We are very grateful to Dave white pelican. Behav Ecol Sociobiol 39:203–209 Anderson, Scott Forbes, Alejandro Gonzalez, Barb Glassey, Evans RM (1997) Parental investment and quality of insurance Regina Macedo, Doug Mock and José Luis Osorno for comments offspring in an obligate brood-reducing species, the American on the manuscript; the Mexican Navy for logistical support; white pelican. Behav Ecol 8:378–383 Bernie Tershey for advice on the logistics and boobies of San Evans RM, McMahon BF (1987) Within-brood variation in Pedro Mártir; Jaime Zaldivar for drawing Fig. 2; and Prescott growth and condition in relation to brood reduction in the College for logistical advice and support. The experiment and American white pelican. Wilson Bull 99:190–201 observations were authorized by the Secretaría del Medioambiente Forbes LS (1990) Insurance offspring and the evolution of avian y Recursos Naturales and carried out in accordance with Mexican clutch size. J Theor Biol 147:345–359 law and the ABS/ASAB Guidelines for the Use of Animals in Forbes LS (1991) Insurance offspring and brood reduction in a Research. variable environment: the costs and benefits of pessimism. Oikos 62:325–332 296 Forbes LS, Mock DW (1996) Food, information and avian brood Mock DW, Forbes LS (1995) The evolution of parental optimism. reduction. Ecoscience 3:45–53 Trends Ecol Evol 10:130–134 Forbes LS, Mock DW (1998) Parental optimism and progeny Mock DW, Lamey TC (1991) The role of brood size in regulating choice: When is screening for offspring quality affordable? egret sibling aggression. Am Nat 138:1015–1026 J Theor Biol 192:3–14 Mock DW, Parker GA (1986) Advantages and disadvantages of Forbes LS, Ydenberg RC (1992) Sibling rivalry in a variable envi- ardeid brood reduction. Evolution 40:459–470 ronment. Theor Popul Biol 41:335–360 Mock DW, Parker GA (1997) The evolution of sibling rivalry. Fujioka M (1985) Sibling competition and siblicide in asynchro- Oxford University Press, Oxford nously hatching broods of the cattle egret Bubulcus ibis. Anim Nelson JB (1978) The Sulidae: gannets and boobies. Oxford Behav 33:1228–1242 University Press, London Gargett V (1978) Sibling aggression in the black eagle in the Nuechterlein GL (1981) Asynchronous hatching and sibling com- Matopos, Rhodesia. Ostrich 49:57–63 petition in western grebe broods. Can J Zool 59:994–998 Gerhardt RP, Gerhardt DM, Vásquez MA (1997) Siblicide in O’Connor RJ (1978) Brood reduction in birds: selection for fratri- Swallow-tailed Kites. Wilson Bull 109:112–120 cide, infanticide, and suicide. Anim Behav 26:79–96 Godfray HCJ, Harper AB (1990). The evolution of brood reduc- Ploger BJ, DW Mock (1986) Role of sibling aggression in distri- tion by siblicide in birds. J Theor Biol 145:163–175 bution of food to nestling cattle egrets (Bubulcus ibis). Auk Grafen A (1987) The logic of divisively asymmetric contests: re- 103:768–776 spect for ownership and the desperado effect. Anim Behav Ricklefs RE (1982) Some considerations on sibling competition 35:462–467 and avian growth rates. Auk 99:141–147 Hollander M, Wolfe DA (1999) Nonparametric statistical meth- Simmons R (1988) Offspring quality and the evolution of cainism. ods. Wiley, New York Ibis 130:339–357 Kasuya E (2001) Mann-Whitney U test when variances are un- Stinson CH (1979) On the selective advantage of fratricide in rapt- equal. Anim Behav 61:1247–1249 ors. Evolution 33:1219–1225 Kepler CB (1969) Breeding biology of the blue-faced booby Sula Tershey BR, Breese D, Croll DA (2000) Insurance eggs versus ad- dactylatra personata on Green Island, Kure Atoll. Publ Nuttall ditional eggs: do brown boobies practice obligate siblicide? Ornithol Club 8:1–97 Auk 117:817–820 Meyburg BU (1977) Sibling aggression and cross-fostering of Trivers RL (1974) Parent-offspring conflict. Am Zool 14:249– eagles. In: Temple SA (ed) Endangered birds. University of 264 Wisconsin Press, Madison, pp 195–201 Werschkul DF, Jackson JA (1979) Sibling competition and avian Mock DW (1984) Infanticide, siblicide and avian nestling mortali- growth rates. Ibis 121:97–102 ty. In: Hausfater G, Hrdy SB, (eds) Infanticide: comparative Woodward PW (1972) The natural history of Kure Atoll, North- and evolutionary perspectives. Aldine, New York, pp 2–31 western Hawaiian Islands. Atoll Res Bull 164:1–318