Exploring the Cause of Sexual Dimorphism in the Galapagos Great Frigatebird

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 


Leila Ehsani

Darwin, Evolution, and Galapagos

13 October 2003

 

 

 

Introduction:

 

Great frigatebirds are sexually dimorphic—the male possesses a magnificent red gular sac that inflates during courtship, which the female lacks. Sexual dimorphism is unusual in the Great frigatebird for two reasons.

First, the Great frigatebird is a “socially and genetically monogamous seabird” (Dearborn and Ryan 2002: 307), whereas sexual dimorphism more often occurs in polygamous birds whose breeding success with multiple mates depends on elaborate secondary sexual traits. In a socially and genetically monogamous seabird, one would expect mutual mate preferences, however the female Great frigatebird is extremely picky in choosing her mate (Dearborn and Ryan 2001: 307).

Second, secondary sexual ornamentation in one sex is usually linked with “disproportionately great parental effort by the other” (Dearborn, Anders, and Parker 2002: 746). In the great frigatebird, however, both the male and the female invest equal time and effort in rearing their chicks. If this is the case, then what are the causes of sexual dimorphism in the Great frigatebird; what role has sexual selection played in the evolution of the gular sac; and what, if any, challenges does the Great frigatebird’s brilliant ornamentation pose for conservation today?

This paper explores sexual dimorphism in the Galapagos Great frigatebird. After providing some general information on Great frigatebirds, it will describe the intricate display behavior of these birds. Following this will be a discussion of why sexual dimorphism is unexpected or strange in this species, accompanied by an exploration of two of the leading hypotheses on this matter. Finally, a discussion of conservation will ensue.

What are Great Frigatebirds?

 

Great frigatebirds, Fregata minor, belong to the family Fregatidae. There are five species of frigatebirds worldwide, with only two—the Great and magnificent frigatebirds—inhabiting the Galapagos Islands. The table below describes the main differences between the males and female Great and magnificent frigatebirds.

 

 

 Key Features

 Fregata minor

 Fregata magnificens

 Male

Call

 gobble

 rattle

 Scapular Feathers

 green irridescence

 purple irridescence

 Female

Color of Eye Ring

 red

blue 

 Throat and Breast

 white

 black throat & white breast

 Juvenile

 Face and Throat

 rust-tinged

 white

 

(Rothman, 2003)

 

While Great frigatebirds can be sited throughout the Galapagos, major breeding sites exist on Genovesa, North Seymour, San Cristobal and Espanola Island (NG).

 

Sexual Selection:

 

Darwin described sexual selection as the “struggle between the males for possession of the females” (Darwin 2001: 88). He explained that in species in which the males and females look different despite possessing similar habits and behavior, sexual selection is most probably at work (Darwin 2001: 89). Sexual selection thus leads to sexual dimorphism, defined simply as any phenotypic difference between sexes. Great frigatebird males have two striking morphological ornaments that females lack: a ruff of long iridescent feathers on the back of the neck and a red inflatable throat pouch, which both suggest sexual selection. There are two ways that sexual selection can lead to sexual dimorphism. The first is through male-male competition that entails fighting for access to females, and the second is through mate choice (Wilson, 2003). In the case of the Great frigatebirds, sexual dimorphism probably came about due to mate choice since there is minimal male-male competition because males are not territorial (Nelson 1975: 141).

 

Display Behavior:

 

Great frigatebirds forage pelagically and gather on small remote islands to breed. Males arrive at the island sooner than females and begin performing courtship displays as females arrive to evaluate mates. Males display to females by inflating their brilliant gular sec, which takes from 10-15 minutes to inflate, erecting the iridescent ruff, tilting and wagging the head and throat pouch, extending, shaking the wings, and vocalizing.

 

 

 

 

 

 

 

 


A male frigatebird showing off his inflated gular pouch on North Seymour. (This is a Magnificent, not a Great frigatebird. Even though there are several differences between the two species, their gular sacs are the same).

 

 

 

 

 

 

 

 

 

 

 


The same male extending his wings as a female flies above.

 

Displays are conducted while males are perched in bushes.

 

 

 

 

 

 

 

 

 

 


A female flies above a displaying male on North Seymour. Other birds can also be seen occupying the breeding colony.

 

Females choose mates by first making low inspection flights around the colony and then making closer inspections by landing next to individual males. When a female flies over a group of males, they erupt in display. A particular male continues to display intensely if a female lands next to him for closer assessment. At times, hundreds of males display together, allowing females to quickly and effectively evaluate a wide range of males (Nelson 1975: 117).

 

 

            After a female has chosen a mate, the pair builds a nest together, with the male bringing sticks to the nest site and the female constructing the nest. When the nest is complete, the female lays a one-egg clutch. Males and females breed every two years, presumably an adaptation to the unpredictability of food resources and the long time that it takes to rear the chick (Nelson 1975: 129).

 

Why is Sexual Dimorphism Unexpected or Strange in Great Frigatebirds?

 

Sexual dimorphism more often occurs in: polygamous birds whose breeding success with multiple mates depends on elaborate secondary sexual traits, and in species in which the female invests more heavily in parental care (Dearborn, Anders, and Parker 2001: 746). According to R. L. Trivers, differences in parental investment will cause the higher investing sex to become limiting and will favor the evolution of choosiness in that sex. The nonlimiting sex will compete for the limiting sex and will be relatively unselective in mate selection. For species in which males possess extravagant ornaments, females typically exert mate choice (because of the high, initial cost of producing eggs) and subsequently provide most or all of the parental care. In contrast, species that lack sexual ornaments demonstrate balanced parental effort by males and females (Kokko and Monaghan 2001: 159). Part of the explanation for this is that if males do not contribute to parental care, their reproductive success becomes more heavily dependent on their mating success, leading to more intense male–male competition or more selective female choice (Dearborn, Anders, and Parker 2002: 746). It is precisely by these two pressures that sexual selection can lead to the evolution of sexual dimorphism in a species. In great frigatebirds, however, not only are males socially and genetically monogamous, but they also invest equal effort as females in incubating and rearing the chick.

 

 

 

 

 

 

 

 

 

 


A male frigatebird sharing in parental care (Genovesa)

 

Therefore, the first reason why sexual dimorphism is unexpected in the Great frigatebird is because it is a “socially and genetically monogamous seabird” (Dearborn and Ryan 2002: 307): Great frigatebirds exhibit short-term social monogamy, forming pair bonds that last for the duration of a breeding attempt, and genetic monogamy, since extrapair fertilizations are extremely rare (Dearborn, Anders, and Parker 2002: 746).

The second reason why sexual dimorphism is unexpected in the Great frigatebird is because both the male and female invest equal time and effort in incubating and rearing their chick (Dearborn, Anders, and Parker 2002: 746). Males gather all of the nest material; they incubate for almost half of the 2-month incubation period; they share in brooding the chick for 4–6 weeks; and they contribute extensively to feeding the chick for approximately 8 months (Nelson 1975: 129). While there may be hidden costs on the part of the female that might explain the male’s elaborate ornamentation within the traditional parental investment framework, this seems unlikely since males do not take advantage of any such lack of costs (being monogamous seabirds). 

Below is a phylogeny of frigatebirds and related taxa. What is even more unusual about sexual dimorphism in frigatebirds is that all taxa shown below are characterized by biparental care, but only the frigatebirds have pronounced sexual dimorphism. 

 

 

 

 


           

           

 

 

 

 

 

 

 

 

 

 

 

(Dearborn, Anders, and Parker 2002: 747)

 

 

If this is so, how did sexual dimorphism evolve in Great frigatebirds?

The answer does not seem to be clear: Don Dearborn, an expert on Great frigatebirds recently stated: “The current and historical importance of male ornaments in frigatebirds remains unclear (Dearborn and Ryan 2002: 313).” However, there are two leading hypotheses that this paper will discuss.

 

Hypothesis 1: The Darwin-Fisher Theory

 

To recap, the first reason why sexual dimorphism is unusual in Great frigates is because they are a “socially and genetically monogamous” species and male secondary sexual traits reach their extreme in polygamous species of birds. Male sexual ornaments, however, are often exhibited by monogamous species as well. Darwin recognized this dilemma. Fisher expanded upon his idea, which is why it is now called the Darwin-Fisher theory. This states that the presence of male ornamentation in monogamous birds is selected for by early season breeding by females in good condition. This theory proposes that:

1. Males arrive at the breeding site first;

2. When the first females arrive, all males are available to be chosen as mates;

3. Early-arriving females are in better nutritional condition than late-arriving females;

4. Early-arriving females make their selection based on sexual ornamentation;

5. Late-arriving females are forced to choose males with less exaggerated ornamentation, therefore,

6. Males with exaggerated features have higher reproductive success because of pairing with females in good condition (Dearborn and Ryan 2002: 307).

 

            No precise studies on sexual dimorphism have been done on frigate birds in the Galapagos Islands, but Dearborn and Ryan tested the Darwin-Fisher theory on Great Frigatebirds in the Tern Islands in Hawaii in 1998. If the Darwin-Fisher theory is correct, reproductive success should decline over the season (because early-breeding females that arrive earlier should have better reproductive success due to their better condition), and males with more exaggerated secondary sexual features should be chosen first. Consistent with the Darwin-Fisher theory, Dearborn and Ryan found that reproductive success did decline over the season.

 

 

 

 


                                                                                                                

 

 

 

 

 

 

 

 

 

 

 

 

(Dearborn and Ryan 2002: 310)

 

 

As shown by the above graph, early season nests were more likely to hatch than late season nests, however, males with more exaggerated ornaments were not chosen as mates earlier in the season than males with less exaggerated ornaments. They tested throat pouch color value (darkness or lightness), throat pouch color chroma (saturation of color), iridescent ruff length, and iridescent ruff brightness and found that there was no relationship between the date of egg laying and any male-specific ornament or a combination of these ornaments (Dearborn and Ryan 2002: 310)

 Therefore, the second part of the Darwin-Fisher theory, namely that males with more exaggerated secondary sexual features should be chosen first, was not supported. Dearborn and Ryan measured reproductive success as a component of fitness, and since reproductive success declined over the season, and males with more exaggerated ornaments were not selected earlier, no link was found between exaggerated ornaments and reproductive success.

The Darwin-Fisher Theory was thus not supported. If this study was accurate, this theory fails to explain sexual dimorphism in frigatebirds. This is because even if females in good condition arrive early, and reproductive success does decline over the breeding season, if a female will not pick a frigatebird with more exaggerated ornamentation over another, then it is useless in explaining the evolution of sexual dimorphism in frigatebirds. Even so, perhaps their study was not accurate. Could there have been human limitations on measurement? Some birds can see into the UV spectrum, and thus might have incorporated this into mate choice decisions. Perhaps the study was carried out in an unusual year and in a population that was too small. Furthermore, perhaps Dearborn and Ryan picked the wrong characters to test. Perhaps mate choice in the Great frigatebird has nothing to do with pouch value or chroma, but is instead dependent on the size, symmetry, and perfection of the pouch. The sounds that male frigatebirds make and the movement of their head and wings might also factor into mate choice.

            Dearborn and Ryan suggest that sexual ornamentation was the basis for female choice in the past, but not now. This suggestion begs the question because even if it was the basis of choice in the past, how did sexual dimorphism evolve then? There also seems to be no reason for this to be the case in the past, but not in the present. Their second suggestion, that

female choice might be based on display behavior or intensity rather than on exaggerated secondary sexual ornaments, is a bit stronger. Perhaps female choice is based both on secondary sexual ornamentation and display behavior.

Hypothesis 2: The Operational Sex Ratio Theory                                                                              

To reiterate, the second reason why sexual dimorphism is unusual in Great frigates is because they exhibit biparental care. Mutual mate preferences are expected in species with biparental care, but in the Great frigatebird, the female is choosy. Therefore, a second possible driving force in the exaggeration of male traits in frigatebirds is a male-biased operational sex ratio. This means that at any given time, there may be more males available for mating than there are females, which if true, would lead to female choosiness. Thus variance in male reproductive success would result from differential male success at attracting a social mate (Dearborn, Anders, and Parker 2001: 748).

 

 

Again, no studies have been done specifically on this hypothesis in the Galapagos, but Dearborn, Anders, and Parker tested the Operational Sex Ratio (OSR) theory in Great frigatebirds in the Tern Islands in Hawaii in 1999. The definition of OSR that they used was the “ratio of males currently performing mate-attraction behaviors to females currently involved in mate-searching or ornament evaluating behaviors” (Dearborn, Anders and Parker, 2001: 748). They found that the OSR was heavily biased. There were typically 5 or 6 males to females engaged in display behavior throughout the entire breeding season. A strongly male-biased OSR could be a selective force driving sexual dimorphism in frigatebirds. If this hypothesis is correct, sexual dimorphism may have evolved in Great frigatebirds due to female choice. And if this is the case, males with more exaggerated sexual characteristics would be expected to be more successful at attracting a mate.

However, more work is needed to determine whether this is really the case, since earlier studies by Dearborn and Ryan demonstrated that males with more exaggerated sexual ornamentation were not necessarily chosen as mates earlier on in the breeding season. As a result, the second hypothesis would also not be supported if males with less exaggerated ornaments were not chosen earlier in the breeding season.

 

Conclusion:

            In this paper, I set out to determine the cause of sexual dimorphism in frigatebirds in the Galapagos Islands. I did not find the cause, but two hypotheses were considered. The Darwin Fisher Theory and Operational Sex Ratio Hypothesis were not supported since both rest on the premise that exaggerated male ornamentation is selected earlier on in the breeding season—this was not found. What was found was that reproductive success declined over the breeding season and that there was a heavily male-biased OSR.

The studies mentioned do not seem accurate in measuring female selection of males with more exaggerated ornamentation. There must be something that females look for when they fly over the displaying males, something that causes them to land next to a specific male after seeing many display together. Mate selection is extremely difficult to measure on human terms, particularly because there are many traits or behaviors that we cannot quantify. More studies need to be done on female selection of male with exaggerated ornamentation. If this is found, it will open the doors to possible conclusions about the origin of sexual dimorphism in Great frigatebirds.

            Mate selection (which is one of the causes of sexual dimorphism in animals) is very poorly understood in Great frigatebirds. To find the cause of sexual dimorphism in Great frigatebirds, more research definitely needs to be carried out—not only on sexual ornamentation, but also on display behavior and intensity. There is a strong suggestion that female choice is based on display behavior. It is not only the gular sac and iridescent ruff that are used in display behavior; the sounds, wing and head movement should also be investigated. It would be useful to devise a method to measure display intensity as well. Research also needs to be carried out on elements of group display behavior, not only individual display behavior, because it has been suggested that males in bigger groups tend to be more successful at obtaining a mate. It is only through more research and perhaps through a humble understanding that we might not be able to discover the exact mechanism of sexual selection in these wonderful birds that we may uncover the cause of sexual dimorphism in the Great frigatebirds on the Galapagos Islands.

 

Conservation Considerations:

 

Fortunately, from a conservation point of view, Great frigatebirds have few, if any, predators. As a result, they have a long lifespan, with some birds that Dearborn and Ryan studied living up to thirty-seven years (Dearborn and Ryan 2002: 747). On Genovesa, short-eared owls have been found to kill a few frigatebird chicks, but apart from that, most egg losses are due to disturbance by other male frigatebirds (Reville 1988: 257). It therefore seems that the evolution of the brilliant ornamentation in these birds pose little, or no challenge for conservation efforts today.

Regarding the implementation of any future environmental policies concerning these birds, however, it is important that we do not consider them merely as general pelagic seabirds. The nature and behavior of Great frigatebirds is truly unique—the anomalous evolution of sexual dimorphism in these birds, as well as their distinct foraging techniques such as piracy, set them apart from other typical pelagic seabirds. The evolution of sexual dimorphism in the Great frigatebird suggests that there are aspects of parental investment or feeding strategies that other related seabirds do not share. As a result, it is imperative that further research is conducted on these unique seabirds to ensure that informed conservation decisions are made.

Bibliography

Darwin, Charles. On the Origin of Species. A facsimile of the First Edition. Harvard University Press: USA. 2001.

Dearborn, D.C., A.D. Anders, and P.G. Parker. 2001. Sexual Dimorphism, Extra-Pair Fertilizations, and Operational Sex Ratio in Great Frigatebirds (Fregata minor). Behavioral Ecology 12 (6):746-752.

Dearborn, D. C. and Ryan, M. J. 2002. A Test of the Darwin-Fisher Theory for the Evolution of Male Secondary Sexual Traits in Monogamous Birds. Journal of Evolutionary Biology 15 (2), 307-313.

 

Frigate Birds on San Cristobal. Noticias de Galapagos 28: 3. Anon (NG).

 

Kokko, Hannah and Monaghan, Pat. 2001. Predicting the Direction of Sexual Selection. Ecology Letters 4: 159-165.

 

Nelson, J. B. 1975. The Breeding Biology of Frigate Birds: A Comparative Review. Living Bird 14: 113-156.

 

Pelicaniformes. Rothman, Robert. 12 Sep. 2003 <http://www.rit.edu/~rhrsbi/GalapagosPages/Frigatebirds.html>.

 

Reville, B. J. 1988. Effects of Spacing and Synchrony on Breeding Success in the Great Frigatebird (Fregata minor). AUK; v:105, no.2: 252-259.

 

Sexual Selection. Wilson, Mark V. H. 12 Sep. 2003 <http://www.rit.edu/~rhrsbi/GalapagosPages/Frigatebirds.html>.