The “cycle of violence” hypothesis implicates child abuse as a cause of later violent behavior via social transmission between generations. It has received mixed support from human research and has prompted the study of nonhuman models with comparable abuse behaviors. The underlying biology of child abuse remains a controversial subject, perhaps partly because in nonhuman animals similar behavior occurs relatively rarely in wild populations. The Nazca Booby (Sula granti), a colonial seabird, provides a nonhuman model in which maltreatment of nonfamilial young is widespread under normal living conditions. Essentially all adults show social attraction at some point in their lives to the offspring of other parents, often with a sexual and/or aggressive motivation. Here, we show a correlation between the degree to which a young bird is targeted by such adults and its own infliction of maltreatment later in life. The results provide the first evidence from a nonhuman of socially transmitted maltreatment directed toward unrelated young in the wild.
According to the “cycle of violence” hypothesis, traumatic abuse or neglect of developing young predisposes the maltreated individuals to exhibit the same maltreatment as adults.1 The vast majority of the literature on this topic covers the human situation or captive nonhuman mammals.2,3 We are aware of no studies of intergenerational transmission of maltreatment behavior in birds. However, colonial bird species provide an important opportunity to test the cycle of violence model because nestlings experience aggressive and even sexual maltreatment from adults and larger nestlings.4–6 These nestlings can often be recognized later in life by leg bands or other identifiers, allowing study of their own adult social behaviors. We tested the cycle of violence hypothesis in a colonial seabird, the Nazca Booby (Sula granti), a species in which nestlings regularly experience abusive visits from nonfamilial adults,4 and which show high natal philopatry7 We documented the exposure of nestlings to these visits, and then years later evaluated their behavior as adults in the same colony.
Nazca Boobies raise solitary nestlings on the ground in dense colonies, and frequently leave their offspring unattended while foraging for them at sea. During that time, nonbreeding adults (i.e., those that had not attempted to breed or had tried and failed) seek out unguarded nestlings for social interaction.4 These nonparental adult visitors (NAVs) express a suite of behaviors dominated by aggression but also including affiliative and sexual acts, and virtually all nestlings experience at least one interaction.4,8 Both males and females show all types of NAV behavior, including male-typical copulatory behavior. Siblicidal behavior at hatching reduces 2-chick broods to 1-chick9 and is associated later in life with an elevated frequency of NAV behavior compared with products of 1-egg clutches and 2-egg clutches from which only 1 egg hatched.9 This association implicates testosterone surges experienced during sibling conflicts as an organizing agent for adult abuse of unrelated nestlings,8 in addition to its probable activational role in siblicide.10 However, the ubiquity of NAV behavior among both siblicidal and nonsiblicidal individuals indicates that additional causes exist. We hypothesized that exposure to NAVs as a nestling may program a predisposition toward NAV behavior as an adult, in alignment with the cycle of violence hypothesis.
We collected daily breeding data, including band numbers of family members and siblicide history, and conducted systematic observations of NAVs in a subsection of a breeding colony on Isla Española, Galapagos Islands (1°23.4′S, 89°37.2′W), during three breeding seasons (2000–2001, 2001–2002, and 2002–2003; see Online Supporting Materials). During these observations, one or two observers walked back and forth along the edge of the “Study Area,” scanning for NAVs with nestlings (“NAV events”). If a parent is present, it chases NAVs from the vicinity of the nest.4 Thus, NAVs search for unguarded nestlings between roughly 30 and 80 days of age,4 and this focused search behavior, their unique leg band numbers, their characteristic behavior when visiting a nestling, and the nestlings' reaction to them all distinguished NAVs from biological parents. The topography of the Study Area is flat and open, with clear lines of sight, so NAV events were detected as they began or shortly after. Our observations were facilitated by the fact that Nazca Boobies at this site are indifferent to close human presence. We made these observations daily from roughly 1300 to 1700 hours, when most NAV events occur,4 during January–March, when most nestlings pass through an age-related window of vulnerability to NAVs.4 Because NAV events were rare outside each season's period of observation, each nestling's history as a target of NAV behavior is essentially comprehensive.
The relationship of frequency of nonparental adult visitor (NAV) behavior as an adult to three potential predictors, as determined by a generalized linear mixed-effects model for overdispersed Poisson regression. Each analysis included one or two predictors measured when the bird was a nestling (NAV events experienced by the focal bird and/or whether the focal bird was siblicidal), a random effect that accounts for how frequently the bird was present in the colony as an adult during the observation period, and an observation-level random effect that corrects overdispersion in the Poisson response variable. Significance (indicated by bold type) was determined using the false discovery correction for multiple comparisons.26,27 To implement that correction, analyses are ranked by P value, and di equals the αcrit multiplied by the quantity (P value rank/n), with n equal to the number of P values estimated (in this case, 9). The largest P value less than the corresponding di value is considered significant (αcrit = 0.05), as are all smaller P values.26,27
During 2004–2005, we used the same methods to collect the same data from 24 of these birds as nonbreeding adults, documenting any NAV behavior as a perpetrator; the observers were blind to the history of these 24 birds and knew only that each one's history had been documented. Early in the 2004'2005 breeding season, we placed a conspicuous blue numbered leg band on each of the 24 focal birds to make them easily recognizable. Frequencies of aggressive, affiliative, and sexual behaviors were correlated strongly in these 24 birds as adults in 2004'2005 (ragg—aff = 0.783, P < 105; raff—sex = 0.794, P < 10-5; raff—sex = 0.883, P < 10-5), which suggests that NAV behavior is a unified syndrome rather than separate phenomena rooted in different causes. As predicted by the cycle of violence hypothesis, the number of NAV events that a nestling experienced showed strong positive relationships with the frequency of that individual's NAV behavior as an adult in 2004–2005, considering the total number of events experienced and also the frequencies of the three behavior types individually (Table 1 and Fig. 1), after controlling siblicidal experience. Because NAVs visit only nonfamilial young, these correlations imply that intergenerational transmission of the behavior is at least partially nongenetic.
The high predictive ability of affiliative experience may be surprising, because aggressive and sexual behaviors may seem more invasive to the nestling. However, affiliative behavior is a good predictor of aggressive and sexual behavior, so nestlings can reliably assume that affiliative behavior presages more invasive maltreatment. Indeed, nestlings adopt the submissive “pelican posture” during all three types of interaction, which imposes thermoregulatory stress during the hottest part of the day by making evaporative cooling by gular fluttering impossible.4
The high repeatability of NAV behavior within adult individuals reveals it as a persistent characteristic of individual personality. For the two seasons with adequate samples (2002–2003 and 2004–2005), repeatability11 (r) of the total number of NAV events recorded was 0.31 (n = 176, P = 0.000002). Separated into the three behavior types, repeatabilities were similarly high (affiliative: r = 0.35, P = 0.00002; aggressive: r = 0.30, P = 0.00005; sexual: r = 0.21, P = 0.005). The apparent conditioning of adult behavior by nestling experience (as a target of NAVs and as a participant in siblicide8) is, thus, likely to be lifelong, and may affect other aspects of personality.
The 24 nestlings experienced 0–31 NAV events as targets and perpetrated 1–56 events in 2004–2005, which indicates that adult behavior reflects the degree of their target experience in a continuous, rather than a qualitative, manner (Fig. 1). We found no significant associations between the frequency of NAV events experienced by nestlings and age or body condition at fledging, which suggests that social stress, rather than condition-related stress, drives the pattern of NAV behavior (Table 2). Our observations of these individuals do not suggest a role for any other variable in the association of nestling experience and adult behavior, except for parent attendance: nestlings that are guarded more by their parents experience fewer NAV events and perform fewer events later in life.4 However, this correlational study cannot exclude a role for other variables.
This study and our earlier work8 indicate that two different aspects of the nestling social experience condition this conspicuous element of adult behavior. The siblicide experience is ephemeral but intense, because it is a fight to the death,10 and was revealed as a strong predictor of a NAV's behavior in 104 adults.8 In the present study, a bird's history as a target of NAVs proved to be a much stronger predictor of its adult behavior than was its history of siblicide. (In fact, siblicide history did not reach statistical significance; we attribute that outcome to the much smaller sample size [n = 24] in the present study.) As we suggested with regard to the androgen surge that accompanies siblicidal behavior,8 the intergenerational transmission of NAV behavior indicated by our present results may reflect an organizational effect of socially induced endocrine perturbations. We are focusing on the stress hormone corticosterone and the hypothalamic-pituitary-adrenal (HPA) axis as a probable candidate for physiological mediation of the cycle of violence in this species.12
The proximate-level causation of NAV behavior implicated by the separate cycle of violence and siblicide effects may provide a sufficient explanation for the phenomenon, without invoking any ultimate causation. A possible proximate-level scenario involves the prior evolution of adaptive siblicide under selection within an “insurance” framework.9,13–15 Siblicide as a nestling appears to predispose Nazca Booby adults to NAV behavior,8 so the behavior could come into existence by this means. Thereafter, both the siblicide effect and the cycle of violence can induce NAV behavior. In fact, intergenerational transmission may cause positive feedback: a single NAV can interact with many nestlings and, presumably, induce the NAV phenotype in all of them. An increase in the frequency of NAV behavior could occur over time under this scenario in the absence of selection for the behavior, and could even cross species boundaries: Nazca Booby NAVs also visit and maltreat Blue-footed Booby (S. nebouxii) nestlings16 and could introduce a separate cycle of violence in that species. Members of at least one Blue-footed Booby population exhibit NAV behavior at a lower frequency.8 Of course, selection could act on NAV behavior, either favoring or disfavoring it in adults, and future work will explore this possibility. The behavior certainly has a negative effect on target nestlings, leading indirectly to fatal ectoparasitic bloodfeeding by land birds in some years,4 although growth is apparently not affected (Table 2).
Results of mixed-effects regression predicting five indicators of growth, with nonparental adult visitor (NAV) events experienced as a nestling as a predictor and nestling sex and clutch size as random effects, for all 139 nestlings in the 4-year study. Degrees of freedom were 138 in all cases. “1% down age” is the age of the nestling when only 1% of its downy plumage remained, the rest having been replaced by pennaceous feathers. All measurements were taken on the day that the nestling reached the 1% down stage.
Colonial birds may be a powerful model to study intergenerational transmission of maltreatment. The physical proximity among birds in a colony facilitates encounters among vulnerable youngsters and older, behaviorally dominant individuals. Young birds in colonies are typically easily detectable if older birds search for them, as is the case in Nazca Boobies.4 Although aggressive targeting of nestlings of colonial birds has long been recognized17 (including that induced by nestlings wandering close to unrelated adults5), sexual interest of adults toward young occurs but is relatively unappreciated. A number of bird species, including colonial taxa, exhibit this type of attraction to nestlings (Table 3). The third element of the behavior of Nazca Booby NAVs, affiliative attraction, may be common but overlooked because it can be mistaken for true parental care. We draw attention to all of these routes of attraction to nestlings, encouraging researchers to exploit these behaviors when they are detected to test the idea that experiences during development mold later social behavior. Of particular interest in the context of the cycle of violence would be the possibility of nongenetic intergenerational transmission of behavior, as is indicated by our results in Nazca Boobies.
Sexual interactions that include copulation and courtship between adults and young in birds.
We thank the Galapagos National Park Service for permission to work in the Park and the Charles Darwin Research Station and TAME Airline for logistical support. The manuscript was much improved by the comments of K. Ashbrook, S. Forbes, and D. Mock. This material is based on work supported by the National Science Foundation under grants DEB 98-06606, DEB 0235818, and DEB 08-42199 to D.J.A. Please see the Supplementary Online Material for details about field and analytical methods (dx.doi.org/10.1525/auk.2011.11008).