Zoe von Gerlach

Professor William H. Durham

October 15th 2018

Why do Nazca Boobies (Sula granti) perform NAV behavior?

Abstract

This research project focuses on Nazca boobies and their Non-Parental Adult Visitor

(NAV) behavior. Non-breeding adult Nazca boobies will go to a nest that is not their own to interact with the unattended chick whose are out foraging for food. This interaction can either be playful, aggressive or sexually abusive (Tarlow et al 2001: 1). The purpose of this research project was to examine three different hypotheses dealing with the reasons why NAVs perform this behavior, looking specifically at whether male adult Nazca boobies are more aggressive than females and the reasons behind this. Through the literary research conducted, it was concluded that females are actually much more aggressive than males. The different factors influencing the frequency of NAV behavior as an adult include siblicide and personal victimization as a chick. Although these factors influence NAV behavior, it is likely that high hormone levels at birth and young age have organizational effects that cause this phenomenon in grown Nazca boobies.

Introduction

Figure 1: Map highlighting Sula granti’s range of occurrence (IUCN Red List)

There are three native booby species to the Galapagos. The Red-footed booby, the Blue- footed booby and the Nazca booby. The focus of this project is the Nazca booby. They exhibit two special behaviors that make them so fascinating for to study. Firstly, they practice obligate siblicide. Although the typical clutch size of a Nazca booby nest is 2 eggs, only one hatchling ever

reaches adulthood. The reason the

female lays two eggs is out of

insurance, since their hatching

success rates are only around 60%.

However, if both eggs hatch, then the

stronger will always kill the

weaker one (Ferree et al 2004: 1).

The second behavior Nazca boobies exhibit is NAV behavior. This typically happens when the chick is between 20 and 80 days old, young enough to not be able to defend itself but old enough that its parents leave it alone while foraging for food. These NAV interactions take one of three forms, either the interaction is playful, aggressive or sexually abusive. If the interaction is playful, the adult NAV will bring pebbles or feathers to the chick’s nest and play with it, exhibiting parental behavior. The aggressive interaction often involves jabbing and biting the chick as well as other types of aggressive advances. The sexually abusive interaction is the least common of the three, and involves the adult NAV trying to copulate with the chick (Anderson et al 2004: 1).

One effect of aggressive NAV behavior is that it can indirectly lead to a chick’s death. The wounds created by the NAV attract landbirds to feed blood from the chick. This weakens the chick, and often results in its death (Anderson et al 2004: 3).

This paper will assess three hypotheses and examine published literature to evaluate and asses them.

Hypotheses

1. Adult male Nazca boobies that were abandoned by their female partner take out their

frustration on young chicks through aggressive behavior

2. To improve their own chances of finding a mate, NAVs injure young chicks to reduce the

chick’s physical appeal once they are grown (reducing the attractiveness of the

competition)

3. Female NAVs have a higher percentage than males of exhibiting playful behavior towards

chicks. This is caused by a combination of motherly instinct and hormones, specifically

androgen

Method

There was no personal research conducted for this paper. Instead, this paper is an in depth literature review of published peer-reviewed studies on the subject. All figures are taken from these studies.

All photographs were taken personally. When we were in the Galapagos, chicks had already matured enough to defend themselves against NAVs, so sadly there are no personal photographs of this specific phenomenon to contribute.

Hypothesis 1

Adult male Nazca boobies that were abandoned by their female partner take out their frustration on young chicks through aggressive behavior

Findings

Figure 2: Graph showing the number of females and males committing aggressive NAV events

(Tarlow et al 2001: 4)

This hypothesis is not correct. Firstly, as figure 2 shows, female NAVs are actually more aggressive and more frequently aggressive than male NAVs (Tarlow et al 2001:4). Subsequently, they are also more often the indirect cause of the chick’s death.

To see examples of males acting extremely aggressively, we have to look more closely at mate rotation. In the Nazca boobies, mate rotation is the female’s choice. Sometimes females stay with their breeding partner, but often they will switch to a new one. This allows females to breed with recent non-breeding males that are in better physical and psychological condition. This also results in all females mating, while males go through seasons of breeding and non-breeding. The mate rotation takes one of two forms. Either, the female abandons the male and finds a new mate and a new nest site. Alternatively, the female finds a new mate and together the new mating pair force the old male out of the nesting site. In this instance, the male Nazca boobies do act aggressively as they are trying to protect their nest site. However, the female is on average 15% larger than the male and the male is outnumbered, so the new mating pair successfully takes control of the nest site (Maness and Anderson 2007: 6).

Therefore, male NAVs are not more aggressive than female NAVs, and do not exhibit aggressive behavior towards chicks as a result of mate rotation, but rather exhibit this behavior towards their old mate and their new mating partner. Therefore, the hypothesis did not properly predict the reasons for this kind of NAV behavior, but there are other factors that lead to increased aggression.

Figure 3: Graph showing the number of NAV events committed by failed breeders (Anderson et al 2004: 9)

One reason that adult Nazca boobies exhibit NAV behavior is because of their own failed breeding attempts. As figure 3 shows, 88.2% of failed breeders engage in NAV behavior. (Anderson et al

2004: 10).

Another reason for NAV behavior is victimization. Chicks that were more frequently victims of aggressive NAV behavior were significantly more likely to be aggressive NAVs themselves. During maltreatment, the chick experiences a five-fold increase in corticosterone levels. This cycle of the victim turning into the aggressor leads some people to refer to the phenomenon as a ‘cycle of violence’ (Grace et al 2010: 6).

Figure 4: Graphs highlighting the difference between chicks that committed siblicide and ones that did not, and their subsequent frequency of committing NAV events and aggressive NAV events as adults (Müller et al 2007: 3)

NAV behavior in Nazca Boobies has been compared to NAV behavior in their close relative the Blue-footed boobies. It has also been studied in relation to the practice of obligate siblicide. In Nazca boobies, 60% of fledglings commit siblicide. While committing siblicide, the chick’s testosterone levels sharply increase. Each graph in figure 4 shows two bars, one for 2ECA+ and one for 2EC-. 2ECA+ stands for nests where both eggs hatched and one sibling killed the other one. 2EC- are nests where only one egg hatched and siblicide was not committed by the surviving fledgling. As a result, in these nests the chick did not experience the sharp increase in testosterone levels. The graph shows that the chicks that committed siblicide are more frequent NAVs and more importantly, more frequently exhibit aggressive NAV behavior. This indicates a relation between committing siblicide as a fledgling, experiencing high testosterone levels during one’s youth, and aggressively attacking chick’s that are not one’s own as an adult (Müller et al 2007: 3).

Figure 5: Androgen levels of Nazca and Blue-footed Booby hatchlings (Müller et al 2007: 3)

Figure 5 shows androgen levels of Nazca (NZBO) and Blue-footed booby (BFBO) hatchlings. Blue-footed boobies do not engage in obligate siblicide and are born with lower androgen levels. Nazca boobies on the other hand hatch with higher androgen levels, show higher frequency of NAV behavior, and higher rates of aggressive NAV behavior (Müller et al 2007: 4).

In conclusion, hypothesis 1 is not correct. Males are actually less aggressive than females.

They exhibit aggression towards their old mate and her new mating partner when they are forced out of their nest, but there is no evidence to show that they then go on to be more aggressive towards chicks. Their aggression is aimed at defending their nest site, not taken out on other pairs’ chicks. There are three principle reasons for aggressive NAV behavior, that do not include the abandoned male’s frustration. Instead, the first reason is failed breeding attempts. Another reason is the Nazca booby’s own victimization as a chick, and the resulting exposure to high levels of corticosterone. Thirdly, participating in obligate siblicide and successfully killing one’s sibling, coupled with high androgen levels at birth and sharp increases in testosterone levels while engaging in siblicide, led to higher aggression levels in grown Nazca boobies.

Hypothesis 2

To improve their own chances of finding a mate, NAVs injure young chicks to reduce the chick’s physical appeal once they are grown (reducing the attractiveness of the competition)

Findings

This hypothesis is somewhat correct. Since the Nazca boobies are long lived , the chick and the adult NAV will at one point in their lives compete for mates, and physically injuring them when they are young could reduce the chick’s fitness when it is grown. However, the hypothesis fails to address the main consequence of

NAV behavior.

Figure 6: Chick fates over 4 separate years of study

(Anderson et al 2004: 12)

There is a bigger impact of aggressive NAV behavior: many chicks die as an indirect result of this interaction. The wounds left on the chicks by NAVs attract landbirds to feed on the chick’s blood (Anderson et al 2004: 3). This hinders healing and makes the injuries worse. When mockingbirds bloodfeed on young Nazca boobies, they insert their beaks into the wounds, drink blood and in the process remove small pieces of tissue. Increasing traumatization leads the chick to wander away from the nest and subsequently die far away from their nest site. The amount of bloodfeeding that occurs and subsequently the amount of chicks that die is dependent on rainfall and food availability. In times when food sources are low, the amount of bloodfeeding increases.

(Anderson et al 2004: 11)

There are several benefits to the NAV that result from the death of the chick. If a chick dies, the parents might abandon their now empty nest. This also means that there are two new adult

Nazca boobies available for breeding. The smaller the amount of chicks that reach adulthood also means the smaller the amount of competitors for mates. Therefore, the aggressive advances made by the adult towards the chick could reduce the chick’s fitness, but the primary benefit to the NAV is the chick’s potential death and the numerous benefits associated with it.

Hypothesis 3:

Female NAVs have a higher percentage than males of exhibiting playful behavior towards chicks.

This is caused by a combination of motherly instinct and hormones, specifically androgen

Findings

This hypothesis is completely wrong. First of all, as discussed above and displayed in

Figure 2, female NAVs are much more aggressive and more frequently aggressive than males

(Tarlow et al 2001:4). Females are in no way more playful when it comes to their interaction with chick’s that are not their own.

Figure 7: Corticosterone and testosterone levels in

NAVs and adult non-NAVs

(Tarlow et al 2001: 5)

To examine hormone levels in Nazca boobies, the levels of corticosterone, testosterone, androgen and estrogen were studied in NAVs. As seen in Figure 7, NAVS had higher corticosterone levels after interacting with chicks than adults who did not engage in NAV behavior.

This elevated level of corticosterone could result from a stressful interaction between the adult

Nazca booby and the chick, or the chick’s parents. It could also be an anticipatory response to the potential stressful situation of a returning to the nest (Tarlow et al 2001: 5).

The lower graph in figure 7 depicts the testosterone levels in NAVs and non-NAVs.

Testosterone levels in NAVs were lower after interacting with chicks than in randomly measured non-NAVs. There was no difference between male and female hormone levels detected, and there was no relation between androgen levels and increased aggression levels measured. The difference was only detected between NAVs and non-NAVs (Tarlow et al 2001:5). Therefore, this hypothesis was incorrect. Females are actually more aggressive than males, and there is no evidence to suggest that the hormone levels (at least the ones studied) have an effect on aggression levels in NAV behavior.

New Hypothesis

The study of the three hypotheses outlined above still leaves some questions, the central one being why are female NAVs more aggressive in their interaction with chicks?

The new hypothesis to explain this phenomenon relates NAV behavior back to . Aggressive NAV behavior often leads to the chick’s death. These dead chicks disappear during the night, and William Durham’s new theory is that adult Nazca boobies eat the dead chicks in times of low food availability.

This behavior has been observed in their close relative the brown booby, where it is mostly the females that exhibit cannibalistic behavior (Neves et al 2015: 10). Although Nazca boobies share parental duties, the females have to recover from the high energetic cost of egg production.

This could be one of the reasons that cannibalism is probably more frequent in females than in males. Conclusion

The study of the published literature showed that females are actually much more aggressive and more frequently aggressive than males. The reasons for aggressive NAV behavior, is not as hypothesis 1 stated frustration resulting from abandonment, but failed breeding attempts, victimization as a chick, and siblicide. The primary benefit to the NAV of injuring a chick is not reducing the chick’s fitness, but rather the possible death of the chick. The chick’s death is accompanied by a resulting possibility of acquiring a new nest site, new mate, and eliminating future competitors for mates. Thirdly, female NAVs are not more playful as hypothesis 3 predicted.

Additionally, there is no shown correlation between hormonal androgen levels and aggressive

NAV behavior.

Instead of the reasons suggested by the hypotheses, NAV behavior is likely a hormonal byproduct of obligate siblicide and high androgen levels at birth. Conservation Implications and Recommendations

The IUCN Red List classifies Nazca boobies as least concern. Although their population size is decreasing, they have an estimated population of at least 30,000 individuals (in 2008), and an estimated range of occurrence of 5,8000,000km2 (IUCN).

Further research studies should be conducted to focus on the effects hormones in early developmental stages have on organizational behavior of grown Nazca boobies. Another investigation should focus on tracking chicks that die as a result of NAV behavior to check whether cannibalistic practices take place. This would help us learn more about the proposed new hypothesis, and there is a lot more research that has to go into this topic to understand more about

Nazca booby psychology.

Works Cited

Anderson, D., Porter, E. and Ferree, E. (2004). Non-breeding Nazca Boobies (Sula Granti) Show Social and Sexual Interest in Chicks: Behavioural and Ecological Aspects. Behaviour, 141(8), pp.959-977. Anon, Sula granti . The IUCN Red List of Threatened Species. Available at: http://www.iucnredlist.org/details/22728990/0 [Accessed September 5, 2018].

Ferree, E.D., Wikelski, M.C. & Anderson, D.J., 2004. Hormonal correlates of siblicide in Nazca boobies: support for the Challenge Hypothesis. Hormones and Behavior, 46(5), pp.655–662.

Grace, J. (2014). ENDOCRINE-MEDIATED ORGANIZATIONAL EFFECTS ON PERSONALITY AND STRESS IN NAZCA BOOBIES. [ebook] Winston-Salem, North Carolina: WAKE FOREST UNIVERSITY GRADUATE SCHOOL OF ARTS AND SCIENCES. Available at: https://wakespace.lib.wfu.edu/handle/10339/39247 [Accessed 24 Aug. 2018]. Grace, J. and Anderson, D. (2014). Corticosterone stress response shows long-term repeatability and links to personality in free-living Nazca boobies. General and Comparative Endocrinology, 208, pp.39-48. Grace, J. and Anderson, D. (2018). Early-life maltreatment predicts adult stress response in a long- lived wild . Biology Letters, 14(1), p.20170679. Grace, J., Dean, K., Ottinger, M. and Anderson, D. (2010). Hormonal effects of maltreatment in Nazca booby nestlings: Implications for the “cycle of violence”. Hormones and Behavior, 60(1), pp.78-85. Liang, A., Grace, J., Tompkins, E. and Anderson, D. (2015). Yawning, acute stressors, and arousal reduction in Nazca booby adults and nestlings. Physiology & Behavior, 140, pp.38-43. Maness, T. and Anderson, D. (2007). Serial monogamy and sex ratio bias in Nazca boobies. Proceedings of the Royal Society B: Biological Sciences, 274(1621), pp.2047-2054. Maness, T. and Anderson, D. (2008). Mate rotation by female choice and coercive divorce in Nazca boobies, Sula granti. Animal Behaviour, 76(4), pp.1267-1277. Maness, T., Westbrock, M. and Anderson, D. (2007). Ontogenic Sex Ratio Variation in Nazca Boobies Ends in Male-Biased Adult Sex Ratio. Waterbirds, 30(1), pp.10-16. Müller, M., Brennecke, J., Porter, E., Ottinger, M. and Anderson, D. (2007). Perinatal Androgens and Adult Behavior Vary with Nestling Social System in Siblicidal Boobies. PLoS ONE, 3(6), p.e2460. Müller, M., Porter, E., Grace, J., Awkerman, J., Birchler, K., Gunderson, A., Schneider, E., Westbrock, M. and Anderson, D. (2011). Maltreated nestlings exhibit correlated maltreatment as adults: Evidence of a “cycle of violence” in Nazca Boobies (Sula granti). The Auk, 128(4), pp.615-619. Machado Neves, F. et al., 2015. Cannibalism by Brown Booby (Sula leucogaster) at a small tropical archipelago. Revista Brasileira de Ornitologia, pp.299–304.

Salcedo, S. (2018). Nazca Boobies Offer New Insight into the Mysterious Cycle of Violence that Plagues Humans. [online] Office of Undergraduate Biology | Biology Scholars. Available at: https://biology.cornell.edu/people/sofia-salcedo/ [Accessed 24 Aug. 2018].

Tarlow, E., Wikelski, M. and Anderson, D. (2001). Correlation between plasma steroids and chick visits by nonbreeding adult Nazca boobies. Hormones and Behavior, 43(3), pp.402-407.