ABSTRACT

Sexual selection is the competition seen within a species in order to reproduce successfully.

These pressures in a species have been classified by three different mechanisms: pre-copulation,

post-copulation/pre-fertilization, and post-fertilization pressures. We used these three

classifications to analyze the sexual selection of the blue-footed booby (Sula nebouxii). The

booby is a prime candidate for this study as they have been shown to have intrasexual selection

in both sexes, participate in extra-pair mating, and continually reassess their current pairings.

This study also compared these selection pressures to other seabirds, the Laysan albatross

(Diomedea immutabilis) and the emperor penguin (Aptenodytes forsteri), to show the differences

across species. This uniqueness of the boobies can be seen in their selection of mates by foot

color and courtship dance, but not in their sexual dimorphic calls. We conclude with a call to

action against climate change as boobies reproductive success is intensively linked to ocean

temperatures and food availability.

The importance of sexual selection on a species has been studied since Charles Darwin in his

book published in 1871 called “The descendant of man, and selection in relation to sex.” Since

then, many studies have gone on to support Darwin’s views on sexual selection and continue to

discover more intricacies involved. The basis of sexual selection is due to the competition for

mates in order to successfully reproduce and pass on their genes. Sexual selection can be seen

applied at three separate times: pre-copulation, post-copulation/pre-fertilization, and post-

fertilization (Cunningham and Burkhead 1998). The mechanisms controlling the sexual selection

vary greatly from species to species and many species still remain unstudied. In this paper we

will focus on the topic of sexual selection in relation to the blue-footed booby (Sula nebouxii).

The blue-footed booby is a socially monogamous seabird that is found on arid islands off the

coast of Central and South America (Harris 2001). The booby is widely recognized because both

males and females have blue feet that they used in their courtship displays. After courtship and

copulation, females lay 2 two eggs 5-7 days apart in nests on the ground unlike their close

relatives the red-footed booby that nests in trees (Harris 2001). Once the chicks hatch Tthese

birds practice bi-parental care of the young and take turns feeding and guarding the young chicks

(Nelson 1978). Boobies are monogamous for life and can livegenerally called a long lived

species of birds because they live to around 18 years of age old (Kim et al. 2011).  The sexual

selection pressures in this species were, until recently, thought to be completely based on

intrasexual selection but a study by Torres and Velandon (2005) found it to be mutual selection

in both speciesfemale choice of a male. In this study we aim to focus on the mechanisms of

sexual selection at the 1) pre-copulation, 2) post-copulation/pre-fertilization, and 3) post-

fertilization, in boobies. The main question of this study is: what variables influence the sexual

selection in the blue-footed booby?  We will look to explain this selection by three unique traits

of the booby which are their feet, mating ritual, and calls.

FEET

Foot color-

Female blue-footed boobies use foot color to select their mates and to constantly reassess these

pairings. Foot color plays an important role in this reassessment because the preferred bright

green foot color is also an indicatorive of good health. While blue pigmentation was discovered

to be structural and based entirely on genetics, green has beenwas selected for because yellow

pigmentation in the feet is an indicator that carotenoids are present. Carotenoids are can only be

produced through a good diet and are also essential in the immune system., and cannot be

produced by the boobies themselves. They are derived instead from diet. Therefore, well-fed and

healthy boobies are the only ones that are capable of allocating this yellow pigmentation to their

feet, and are seen as more desirable to the opposite sex. The selection of females for mates with a

greener foot coloration serves as a type of pre-copulation sexual selection. This coloration is

highly susceptible to environmental conditions though, and can take as little as 48 hours to

indicate carotenoids in the diet. change the color of their feet (Torres and Velando 2003).

Velando, Beamonte-Barrientos, and Torres (2006) tested the influence of carotenoids in an

experiment in 2006, after pairs had been established and the first egg was laid. where males were

taken from the nest immediately after the female had laid her first egg in the clutch. The males’

feet were then painted a duller blue color as a signal of “bad health” in accordance with a

previous study by the same authors in 2003.. Upon being returned to the nest and their mates, the

males that were painted were re-assessed by their partners, and the females’ second eggs in the

clutch were laid. On average, Upon return to the nest, the mates of the painted

boobiesexperimental males laid eggs that were smaller in volume than the control males. This,

indicating indicates that they the females had adjusted their level of parental investment based on

the males’ foot color. This example shows that foot color can also be an example of post-

fertilization sexual selection.

There are several reasons females might adjust investment based on the presumed state of their

male partner. Male First, male and female boobies are equal partners in the rearing of chicks. If

the male is presumed to be unfitmalnourished, sickly or old, he cannot do his share in of the

fishing and caring for the chick., leaving the bulk of the burden on the mother. Additionally,

weak males are not desirable donors of genetic material. Old or sickly males’ genetic material is

worth less, and if a female perceives her young are not going to have the best chances, she

immediately lowers her investment. Decreasing the second egg size therefore is very

importanthighly significant, because in broods with two chicks of significantly different sizes the

larger chick will often commit siblicide., kicking its smaller sibling out of the nest. This does not

In blue-footed boobies siblicide will not occur when the chicks are comparable sizes., which is

why females will typically lay a larger egg second if conditions allow. By laying a smaller egg

upon re-assessment of her partner, the female is choosing to only have one chick sired by that

particular father, ensuring she does not waste too many of her own resources caring for

substandard chicks by herself. (Velando et al. 2006).

The parental investment in relation to foot color is also supported by Velando et al. (2005) in a

their cross-fostering experiment where chicks were given to different pairs to raise. Their

condition was comparinged to both the foot color of the foster father and the genetic father. The

results were such that the both fathers’ sexual ornamentation accounted for 32% of variance in

chick condition. This explains why females are so choosy when it comes to male foot color. This

shows that Tthose with brighter, and therefore more attractive, coloration also sire healthier

chicks and prove to be more attentive fathers. (Velando et al. 2005).

Though blue-footed boobies are considered socially monogamous, foot color can also affect the

incidence of extra-pair mates, especially in females. In some cases, females have been observed

engaging in up to seven extra-pair copulations with neighboring males during a single breeding

season. (Osorio-Beristain and Drummond 1998). The occurrence of extra-pair matings has also

been linked to the sexual attractiveness of females, as females with brighter feet have been

shown to attract more extra-pair mates. Males with brighter feet are also less likely to be

cuckolded. (Torres and Velando 2005).

Female ornamentation-

Ornamentation is the use of brightly colored visual displays commonly seen in the males of a

species in order to attract females (Darwin 1871). This form of sexual selection has been

extensively studied and can be observed across the animal kingdom (Amundsen 2000). Female

ornamentation is not as common as males, but it is far from rare. When females adopted the

same elaborate coloration of the males it was thought that to still be driven by female selection,

but the favorable traits were highly heritable and were therefore “accidentally” inherited by the

females. This idea was presented by Charles Darwin (1871) and was called as “the laws of

inheritance”. This type of male and female ornamentation is very apparent in the blue-footed

booby with their auspicious blue feet.  Darwin’s law of inheritance is not widely accepted

anymore as scientists continue to learn more about the role of female ornamentation. In the

aforementioned boobies, a study by Torres and Velando (2005) they showed that females’ blue

feet were a factor in the males’ choice for a partner as female with darker feet participated

significantly less in courtship with their mate (figure 2). This study also showed that the color of

the females’ feet greatly affected the chance of courting with extra-pair mates. More attractive

females were 5.4 times more likely to be courted by a male besides their mate (Torres and

Velando 2005). Males’ choice of a specific female based on foot color is another example of pre-

copulation sexual selection. This mutual selection of males and females has not been well

studied in birds, but has been found to be correlated with bi-parental care and is this is another

likely cause of the boobies mutual ornamentation (Guerra and Drummond 1995, Amundsen

2000). (Amundsen 2000).  Since blue-footed boobies share in the care of their offspring, this is

another likely cause of the mutual ornamentation (Guerra and Drummond 1995).

Bi-parental care and monogamy-

Bi-parental care plays a large role in the monogamous nature of the blue-footed boobyse birds.

Bi-parental care is often an indicator of whether a certain species is monogamous, and the extent

of obligate parental care influences the amount of polygyny within a breeding colony. The level

of breeding synchronicity also influences polygyny in the breeding system, as well as the sex

ratios within a certain colony. Therefore, birds with a longer period of bi-parental care,

synchronous breeding seasons, and even-sex ratios are unlikely to participate in polygyny,

whereas in colonies with uneven sex ratios, asynchronous seasons, or uneven parental investment

will likely have some degree of extra-pair mating. (Tershy and Croll 2000).

A good example of strict monogamy is the eemperor ppenguin (Aptenodytes forsteri). Since their

harsh environment mandates breeding synchronicity and they have an equal amount of

investment by both parents, there is no recorded incidence of extra pair mating in this species.

This is also evidentevidenced by the lack of sexual dimorphism within the species, indicating the

equal nature of a permanently mated male and female pairing. (Jenouvrier et al. 2010) Boobies,

however, do not have this extreme level of synchronicity, and it is suggested that the amount of

breeding synchronicity varies per colony. They also often have uneven sex ratios that make it

easier to engage in extra-pair mating even though they share in parental effort. This is evidenced

by a particularly unusual case study where several blue-footed booby nests were observed being

shared, each time with two females and one male. This unusual group nesting behavior was said

to be a result of more females than males in the breeding colony, and while it resulted in more

females having mates, it did not improve overall breeding success. One trio of parents were

reported to have successfully raised three chicks, while the others either broke up prior to

incubation or abandoned the nest, resulting in no reproductive success. (Castillo-Guerrero et al.

2005)

Though monogamy is favored in marine bird species, there are some trade-offs that suggest

promiscuity can also be beneficial. It has been hypothesized that monogamy evolved in boobies

and other seabirds because their dependence on the ocean mandates one parent tomust leave the

nest for long periods of time, making it impossible to rear the chick without aid from both

parents. Unlike many monogamous seabirds (including other species of boobies), blue-footed

boobies are capable of raising more than one nestling to adulthood. This is due to the fact that

boobies typically live in places where food is abundant, like the Galápagos., and bBoobies are

sexually dimorphic in their size and foraging behavior, with the larger females bringing home

largergreater catches and males foraging more frequently from closer distances. (Wittenberger

and Tilson 1980) However, boobies are not strictly monogamous, and while there are theories

about the benefits of promiscuity and extra-pair mating, it is not certain why blue-footed boobies

developed this behavior. As discussed earlier, Cconstant re-assessment of pairs and the ability to

move on to new partners does allow females to ensure the highest quality of her chicks., as

discussed earlier, and eExtra-pair mating can also serve to increase genetic diversity and ensure

those individuals who were unable to find mates before the abilityalso get to pass on their

genesinformation.

Blue-footed boobies are also interesting because the females are typically up to 30% larger than

males and therefore are the determining sex when it comes to extra-pair copulations. While it is

questionable if that females increase their fecundity by engaging in these behaviors, it is

suggested that females may participate in extra-pair mating during her fertile period to increase

the genetic quality of her offspring. (Osorio-Beristain and Drummond 1998). It is also probable

that male age has an effect on extra-pair mating in females, as male “attractiveness” and overall

fitness decrease as males become senescent at around 10 years of age. As pairs have been known

to spend an average of 5-6 breeding seasons together, it is likely that males become senescent in

this time and increase the likelihood of extra-pair mating by females. (Kim et al. 2011). Taking

on extra-pair mates due to the altered condition of the male is a further example of constant

reassessment of the pair as well as post-fertilization sexual selection.

MATING RITUAL

The Bonds of Dance

Courtship displays are another way that females of a species have been shown to choose their

mates. These dances involve complicated auditory and visual stimuli in the attempt of winning a

mate ( ). These types of courtship rituals can be found in mammals, reptiles, amphibians, fish,

and some insects, but is predominantly found in birds (     ). One such example of this can be

seen in the dance of the Laysan aAlbatross (Diomedea immutabilis). The courtship displays

involves a variable pattern of movements with correlated honks and whistles that are performed

by both the male and females (Meseth 1975). The origin of these movements is thought to be

derived from other behaviors such as nest building, comforting behaviors, and locomotion that

were adapted to serve a reproductive purpose (Meseth 1975).  The dance of the blue-footed

boobies shows many parallels to the Laysan Albatross, with some key differences.

Blue-footed boobies have four main actions in their courtship ritual: landing, presenting nesting

material, parading, and sky-pointing (Nelson 1978). The following description is from a personal

observation made on Isabela Island, Galapagos Islands. The first step is always initiated by a

male where he lands in front of the female with his feet splayed in front of him. He then presents

a gift in the form of a stick or other nesting material to the female. The male then will flaunt his

feet to the female in a high stepping display called parading. This exaggerated stepping is usually

done in conjunction with a high pitched whistled call. The final move of this sequence is a

motion called the “sky point” where the male and female boobies will lift their heads toward the

sky while opening their wings. When a female accepts a male she will follow his lead and

accompany his whistle with her trumpet (Nelson 1978). This dance does not always lead to

copulation, but that is the end goal (Osorio-Beristain and Drummond 1998). The order of these

motions does not vary, unlike the dance of the albatross (Meseth 1975). Similar to the

aforementioned albatross, the motions in the boobies dances have probably transformed from

other behaviors. The presenting of nesting material to the female is most likely derived from dual

parental investment in the raising of the young. The parading must be used to display their blue

foot as it is the main visual cue for sexual selection. The albatross described by Meseth (1975)

also did a motion similar to sky pointing that he attributed to a pre-flight motion. Like the

albatross, boobies are monogamous birds and will perform their courtship dances at the

beginning of a breeding season to reaffirm previous breeding pairs (Meseth 1975).

CALLS

Sexually Dimorphic Calls-

Calls in birds are most commonly used by males to attract a mate, but these signals have been

shown to also be used for mate recognition and pair bond maintenance in many species

(Dentressangle et al. 2012). The call of many penguins species (Spheniscidae) have been shown

to serve all of these purposes (Robinson et al. 1993). Robinson et al. (1993) suggests that the

evolution of these individualized calls was mainly influenced by the noisy environment of the

nesting colonies. Like penguins, Blue-footed boobies are monogamous colonial nesting seabirds

with bi-parental care (Nelson 1978). For these reasons it is also suggested that boobies developed

their individual sexual dimorphic calls. Unlike penguins though, the difference of the calls

between the species is greatly noticeable. Female boobies produce a loud trumpet sound while

males have a high pitched whistle (Nelson 1978). These calls are used during the courtship ritual

as well as a greeting back to the nest after a foraging trip (Nelson 1978). Dentressangle et al.

(2012) showed that calls can vary individually on 10 acoustic variables and that mates could

recognize these minute differences. This recognition is imperative as the main visual cues in the

boobies, their blue foot, are highly variable based on their health status (Torres and Velando

2003). In order to achieve these individualized calls females tend to vary the harmony and pitch,

while males change the frequency of their whistle (Dentressangle et al. 2012). While it is still

unknown why the calls vary between sex, it is thought to be because of the size dimorphism in

of females that are usually 30% larger than males (Dentressangle et al. 2012). It has not been

shown if these calls influence the formation of new pairs, but it is essential to maintain a

breeding pair from year to year. Therefore, unlike other species the call of the blue-footed booby

is not thought to be a pre-copulation form of sexual selection.

Conclusion:

Our goals in this study were to highlight the unique aspects of sexual selection in the blue-footed

booby, as well as determine the devices driving this selection. We also strove to answer the ways

in which sexual selection is manifested in blue-footed boobies, and how these birds are unique in

their mating behaviors in comparison to other marine bird species.

Blue-footed boobies are incredibly unique in their mating behaviors as compared to other

seabirds. Sexual selection by these birds is a multi-faceted process that includes assessment of

foot color by both females and males in order to determine health, virility, and parental

investment in chicks, as well as an evaluation of the potential partner’s courtship dance. Blue-

footed boobies also frequently reassess their partners once mated and throughout their time

together in order to determine parental investment and the frequency of extra-pair mating. Calls,

though important in identification and reaffirming pair bonds, do not play a large role in

courtship like they do in other bird species.

Through our research on mating behaviors in blue-footed boobies, we became aware of how El

Niño and climate change events can seriously impact reproductive success in this incredibly

selective species. In learning about how malnutrition and lack of carotenoids in the system can

result in a failure to court, we realized that El Niño events, which cause serious food shortages,

can seriously reduce mating success. In one paper, it was Wingfield et al. (1998) recorded that

the 1992 El Niño resulted in 100% breeding failure in blue-footed boobies for that year. That

year, ocean surface temperature roseraised an average of 1ºC, yet resulted in less pairs mating

and an 89% abandonment of nests if eggs were laid; of those not abandoned the rest of the chicks

all died before they could fledge (Wingfield et al. 1998). and the resulting lack of food not only

led to malnourishment in adults, but also caused them to have to fly farther in search of food

leading to a shortage of free time to devote to courting and reproducing. (Wingfield et al. 1998)

This led us to look toward the future of blue-footed boobies, as a likely increase in ocean

temperature causeds by climate change will cause a collapse of their whole breeding system to

collapse. Based on this data, we assert that climate change is an enormous potential threat to the

reproductive success of this species, as it is with so many others. We feel that research on these

creatures is invaluable as much is left unknown about them and especially about their sexual

selection. at what we believe is a critical point worldwide. If We believe that this is a critical

point worldwide and if we are to take strides to reduce our global impact, it must be soon, as

even 1ºC can make the difference between life and death for the blue-footed booby.