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.
Beginning in 1999, I have been studying sexual dimorphism in the purple-throated carib (Anthracothorax jugularis), initially 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 (Fig. 1A & B).
In studies with Amherst students Irvin Pan (1999), Jill Brennan (2001), and Jed Horwitt (2001), I found that the purple-throated carib is the sole pollinator of two species of Heliconia, a red-bracted morph of H. caribaea (Fig. 1G), and a green-bracted morph of H. bihai (Fig. 1E) endemic to St. Lucia. Flowers of H. caribaea (Fig. 1D) correspond in size and shape to the bills of male caribs, whereas flowers of the green-bracted H. bihai (Fig. 1C) 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 (Fig. 1F) with flowers matching the bills of males, and a green-bracted morph with flowers matching the bills of females (Temeles et al. 2000 Science).
Subsequently, John Kress, Curator of Botany at the Smithsonian Institution and an 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 morph, which is red with a yellow stripe (Fig. 1H). Heliconia caribaea is more common than H. bihai, and it is the Heliconia species with two color morphs: a yellow-bracted morph (Fig. 1J) with shorter, straighter flowers matching the bills of males, and a red-bracted morph (Fig. 1I) 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 & Kress 2003 Science).
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 (Fig. 2).
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 as Temeles et al. 2004 Condor with honors students Amanda B. Muir, Elon B. Slutsky, and Maren N. Vitousek).
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. (Fig. 3).
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 as Temeles et al. 2005 Auk with honors students Robin S. Goldman and Alexi U. Kudla).
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 analyzed 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 involved 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 was 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 (Fig. 4). 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.
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 (Fig. 5). (This work was published as Temeles et al. 2009 Ecology with honors students Carolyn R. Koulouris and Sarah E. Sander).
In addition to examining feeding performance of male and female purple-throats in the context of natural selection, we examined sexual selection acting on males. Our earlier studies demonstrated a close correspondence between energy rewards of the heliconias and the body size and energy needs of sexes of purple-throats and suggested that natural selection may have had a role in the evolution of body sizes of the sexes (Temeles et al. 2000, 2005; Temeles & Kress 2003). Because male purple-throats also defend heliconias for breeding, however, we noted that sexual selection may have had a role in the evolution of their larger size. In a study of a population of 12 males defending territories of H. caribaea on the island of Dominica, we found that males defended territories greatly in excess of their energy needs, and that females preferred to mate with males having the highest standing crops of nectar on their territories. Males specifically maintained plants on their territories for use by females, a behavior we have termed “flower farming” (see Fig. 6). A male’s ability to accumulate high standing crops of nectar on his territory depended on his ability to evict intruders, as well as on his size, with larger males being the most successful. Thus, sexual selection contributes to the larger size of male purple-throated caribs (this work was published as Temeles & Kress 2010 Proc. R. Soc. B).
The purple-throated carib hummingbird and its Heliconia food plants provide some of the best evidence to date for ecological causation of sexual dimorphism, but also raise the question of whether this evidence is simply an isolated case resulting from ecological release on islands or alternatively is more widespread than previously imagined. The purple-throated carib is absent from the islands of Grenada, Tobago, and Trinidad, even though one of the heliconias it visits, H. bihai, occurs there. Another aspect of our work is to determine what hummingbird(s) replace purple-throats geographically as pollinators of H. bihai (and H. caribaea). Heliconia bihai, on these three islands is a generalist with extremely short flowers pollinated by 3 to 6 hummingbird species per island. We discovered that two of these hummingbirds, the rufous-breasted hermit, Glaucis hirsutus, and the green hermit, Phaethornis guy, have sexual dimorphism in bill curvature similar to that of the purple-throated carib. This discovery prompted a phylogenetic analysis of sexual dimorphism within the hermit hummingbirds (Phaethornithinae) in which we determined that sexual dimorphism in bill curvature is widespread within this subfamily (Fig. 7).
Moreover, our own field observations together with those of Taylor and White (2007 Ornithol Neotrop.) indicate that the sort of sexual partitioning of heliconias we have documented for purple-throats also occurs in many species of hermit hummingbirds, and that ecological causation of sexual dimorphism may be more common than has been previously thought. (Fig. 8). This work was published as Temeles et al. 2010 Phil. Trans. Roy. Soc. B with honors student Joanna L. Rifkin and molecular phylogenetics wizard Jill S. Miller.