Sexual Dimorphism and Floral Polymorphism in a Hummingbird-Plant Association

Sexual dimorphism in size and morphology is widespread in the animal kingdom. Charles Darwin drew attention to these differences, and offered three explanations for their evolution based on mechanisms of sexual selection, fecundity selection, and ecological causation, e.g., resource- partitioning. Although empirical studies demonstrate that the first two mechanisms operate in natural populations, unambiguous examples of ecological causation of sexual dimorphism have been hard to find, because in many animal species, sexual differences in the size of feeding structures scale positively with body size. The positive relationship between body size and feeding morphology makes it unclear whether ecological differences between the sexes are the cause or the consequence of sexual dimorphism.

Since 1999, I have been studying sexual dimorphism in the purple-throated carib (Eulampis jugularis) on the island of St. Lucia, West Indies. Although the wings and body masses of males average 8.6% and 25% larger than those of females, the bills of females average 20% longer and 40% than those more curve than those of males, one of the most extreme bill dimorphisms of any hummingbird.(See picture.)

In studies with Amherst students Irvin Pan [‘99], Jill Brennan [‘01], and Jed Horwitt [‘01], I found that the purple-throated carib is the sole pollinator of two species of Heliconia, a red-bracted H. caribaea, and a green-bracted race of H. bihai endemic to St. Lucia. Flowers of H. caribaea correspond in size and shape to the bills of male caribs, whereas flowers of the green-bracted H. bihai correspond in size and shape to the bills of female caribs. Further evidence for ecological causation of sexual dimorphism (and plant-pollinator coevolution) was provided by a geographic replacement of H. caribaea by H. bihai where the former is rare, and the subsequent development of a floral dimorphism in H. bihai, with a red-green bracted morph with flowers matching the bills of males, and a green-bracted morph with flowers matching the bills of females (see 2000. Science 289:441-443 PDF ). (See picture.)

More recently, John Kress, Curator of Botany at the Smithsonian Institution and a leading authority on Heliconia taxonomy and systematics, and I found additional support for ecological causation of sexual dimorphism in the purple-throated carib from studies on the island of Dominica, 120 kilometers to the north. As on St. Lucia, Dominica has both H. caribaea and H. bihai, with flowers of the former matching bills of males and flowers of the latter matching bills of females. But on Dominica, H. bihai has only one more, which is red with a yellow stripe (See picture.) H. caribaea is more common than H. bihai, and it is the Heliconia species with two color morphs: a yellow-bracted morph with shorter, straighter flowers matching the bills of males, and a red-bracted morph with longer, more curved flowers matching the bills of females. Not only that, but the replacement morphs on Dominica or St. Lucia either reduce (Dominica) or increase (St. Lucia) their nectar reward through decreases or increases in their numbers of bracts and flowers in correspondence to the size and energy requirements of their female or male pollinator. This latter finding suggests that sexual differences in body size of purple-throated caribs, and not just their bill morphology, are maintained by feeding specialization on the different Heliconia food plants (Temeles and Kress. 2003. Science 300:630-633 PDF ).

The roles of food and sex in Heliconia use by purple-throated caribs

Both intersexual food competition and sexual selection may result in male-male competition for territories, either as food sources during the non-breeding period, or as feeding-and-mating territories during the breeding period. Competition between males and females for flowers during the non-breeding season is an unambiguous indicator of intersexual food competition. Because many females that intrude onto male territories during breeding periods copulate with males, however, it is unclear whether male territorial defense during the breeding period is mostly for food, and driven by intersexual food competition, or is mostly for sex, and driven by sexual selection.

To discriminate between these two alternatives for territory maintenance, my students and I experimentally reduced flower numbers on territories of four different males by covering Heliconia flowers with clear plastic bags on male territories in 2000, 2001, and 2002 on the island of St. Lucia. If breeding territories are defended primarily for sex, then experimental reductions of flower numbers on male territories should have little effect on the amount of time a male spends on the territory. This was why we covered bracts with clear bags: if breeding territories are for sex, then clear plastic bags should not reduce territory attractiveness if inflorescences (flower stalks) are a signal of male quality. Alternatively, if breeding territories are defended primarily for food, we expected males to spend more time off of territories feeding following experimental reductions of flower numbers on their territories, as well as lose weight, which we monitored by weighing males with electronic balances fitted to Heliconia inflorescences (See picture.)

Following inflorescence reductions, males reduced the time they spent feeding on their territories and lost a significant amount of weight, but increased their time feeding and regained weight to pre-manipulation levels following restoration of flower abundance. Territorial males also reduced the amount of time they spent in defense and in mating chases following inflorescence reductions. Both results indicate that males derive an energy benefit from defense of Heliconia territories during the breeding season, in contrast to studies of some other hummingbird species. In all three years, significantly more females intruded onto the more rewarding H. caribaea than onto H. bihai territories, suggesting that the quality of a male’s territory may be a cue for female choice of mates in this hummingbird-flower system (This research was published in the Condor 2004, volume 106:691-695.

Sexual dimorphism and foraging and territorial economics at three heliconias

Additional support for the role of food in driving this hummingbird – Heliconia system comes from a study of foraging and territorial economics at the three heliconias on St. Lucia. Across three years of study, H. caribaea territories defended by males were significantly smaller in area and had higher densities of flowers than red-green H. bihai territories, and both kinds of male Heliconia territories were smaller and had higher densities of flowers than a green H. bihai territory maintained by a female (females were rarely observed on Heliconia territories and the single female post-breeding territory was the only female territory found in three years’ of studies). My undergraduate students and I used measured metabolic costs of sleeping, resting, and hovering for purple-throated caribs obtained by Wolf and Hainsworth (1971 Ecology), and Gill’s and Wolf’s (1975 Ecology) equations for territory and foraging economics of sunbirds (modified for the hummingbirds), to estimate the relative costs of foraging and defense for male and female purple-throated caribs at the three heliconias. The smaller territory areas and higher flower densities of H. caribaea territories lowered males’ foraging time and energy costs per flower relative to red-green H. bihai territories, which theoretically allowed them to meet their energy demands in less time and at lower cost. Males’ estimated foraging time and energy costs were greatest at the green morph of H. bihai, and compared to females, they would save a higher proportion of time and energy by foraging at H. caribaea and the red-green morph of H. bihai. (See figure.)This asymmetry in relative gains from foraging at each of the three heliconias for males and females may further reinforce resource partitioning between them, in addition to differences in size and fighting abilities (This research was published in the Auk 2005, volume 122:187-204).

Feeding performance and bill morphology of the sexes

As noted above, sexes of purple-throated carib hummingbirds exhibit extreme sexual dimorphism in bill morphology, with males having short, straight bills and females having bills 20% longer and 40% more curved. We have been analyzing feeding performance of males and females in order to understand how these differences in bill morphology between the sexes contribute to niche partitioning. These experiments involve the use of natural Heliconia flowers on St. Lucia and 34 artificial flowers differing in length, curvature, and diameter. The use of artificial flowers allows us to examine birds’ feeding performance at floral phenotypes not found in nature, and gives us insight into how their bills would respond to selection were there environment to change.

Our most exciting finding to date is evidence for a trade-off in the relative advantages of short, straight bills and long, curved bills. Specifically, the longer, more highly curved bills of female purple-throated caribs allow them to feed from longer, more highly curved flowers than males, and to do so more quickly, when the birds perch on Heliconia bracts to feed (See figure). Males had great difficulty extracting nectar from flowers of the green morph of H. bihai, and in many cases could not insert their bills into flowers of the green morph due to mismatches between bill and flower shape (see video clip).

Experiments with artificial flowers supported those with real Heliconia flowers. Only 1 of 6 males was able to extract nectar from an artificial flower of dimensions 44 mm long x 3 mm wide x 0.04 1/mm curvature, replicating the dimensions of the green morph of H. bihai on St. Lucia visited primarily by females. In contrast, even though the bills of males are much shorter than the bills of females, they could extract nectar from the same maximum length of straight flowers while hovering Moreover, males had significantly faster handling times and better feeding performance than females when hovering to feed from perfectly straight flowers (See figure). See Temeles et al. 2009 Ecology.

[back]