Ethan J. Temeles

The evolution of sexual dimorphism in animals: Hypotheses and tests

Three major hypotheses, based upon mechanisms of sexual selection, intersexual food competition and reproductive role division, have been advanced to explain the evolution of sexual dimorphism in body size and morphology of animals. Genetic models suggest that all of the hypotheses are plausible, and empirical studies demonstrate that each of the three mechanisms operates in natural populations. However, problems arise in testing hypotheses for the evolution of sexual dimorphism: more than one mechanism may be operating simultaneously, and the demonstrated occurrence of a mechanism does not indicate that it actually results in selection for dimorphism. A recent statistical technique offers a solution to these problems and provides a promising new approach to the study of sexual dimorphism, in which researchers can assess the relative importance of each mechanism in present-day selection for sexual dimorphism within a species.

Sexual Size Dimorphism of Bird-Eating Hawks: The Effect of Prey Vulnerability

Among predatory birds, magnitude of sexual size dimorphism increases progressively from carrion-eating and invertebrate-eating species through fish-eating and mammal-eating species to a high in bird-eating species. Analysis of raptor hunting success demonstrates that the relation between hunting success and prey type is exactly opposite the relation between prey type and degree of dimorphism: raptors that prey upon birds experience more difficulty in the successful capture of their prey than raptors that prey upon fish, reptiles, or invertebrates. Consequently, a new hypothesis based upon prey vulnerability is introduced to explain differences in degree of raptor dimorphism. The prey vulnerability hypothesis maintains that lower encounter rates and capture successes resulting from the highly developed predator detection and escape abilities of avian prey may lower the availability of avian prey in comparison to nonavian prey. This would result in bird-eating raptors receiving a lower net energy intake per unit time spent foraging than non-bird-eating raptors. The prey vulnerability hypothesis supplements intersexual food competition or sexual role division hypotheses by presenting an alternative mechanism based upon prey availabilities (not prey abundances) for how differences among prey types may have led to differences in degree of raptor size dimorphism.

Interference asymmetries among age-sex classes of rufous hummingbirds during migratory stopovers

SummaryThree age-sex classes of rufous hummingbirds (Selasphorus rufus) overlap temporally and defend feeding territories during migratory stopovers in the Sierra Nevada of California. We demonstrate that these classes differ in their ability to secure and maintain high-quality feeding territories for refueling, and that these differences result in differences in resource use. Data on acquisition of territories, territory characteristics, and responses of territory owners to intruders suggest that several mechanisms are involved in determining dominance, involving sex- and age-related differences in wing disc loading, coloration, and experience. We discuss the implications of these results for understanding intraspecific variation in migration strategies.

Effect of flower shape and size on foraging performance and trade‐offs in a tropical hummingbird

Matches between the bills of hummingbirds and the flowers they visit have been interpreted as examples of coadaptation and feeding specialization. Observations of birds feeding at flowers longer or shorter than their bills combined with a lack of experimental evidence for foraging trade-offs, however, fail to support these interpretations. We addressed these inconsistencies by considering a seldom-studied dimension of hummingbird-flower relationships, the shape of bills and flowers, through experiments on the Purple-throated Carib, Eulampis jugularis, and its major food plant, Heliconia, in the eastern Caribbean. Bills of male E. jugularis are considerably shorter and straighter than bills of females. We examined foraging performances and trade-offs during visits to natural heliconias and 34 artificial flowers of differing length and curvature. Supporting predictions based on matches between bill and flower morphology, handling times of females were significantly shorter than those of males at the long, curved flowers of a green morph of H. bihai. Contrary to predictions, handling times of males were not significantly shorter than handling times of females at the short flowers of H. caribaea. At artificial flowers, maximum extraction depths of females were significantly longer than maximum extraction depths of males at all curved flowers, but not at straight flowers. Handling times of females were significantly shorter than handling times of males at the longest artificial flowers for all curvatures, whereas handling times of males were significantly shorter at short, straight, artificial flowers, but only while hover-feeding without a perch. Within each sex, handling times were inversely related to bill length at long flowers for all shapes. Taken together, these performance trade-offs suggest that the long, curved bills of females are adapted for feeding from long, curved flowers, whereas the short bills of males are adapted for hover-feeding from short, straighter flowers. In addition, the finding that differences in feeding performance occur at the extremes of floral phenotypes suggests that the evolution of bill morphology may be driven by a small subset of the flowers visited by a hummingbird species.

A new dimension to hummingbird-flower relationships

The close correspondence between the bills of hummingbirds and the lengths of the flowers they feed from has been interpreted as an example of coadaptation. Observations of birds feeding at flowers longer and shorter than their bills, however, and the lack of experimental evidence for any feeding advantage to short bills, seem to contradict this interpretation. I address this problem by considering a little-studied dimension of floral morphology: corolla diameter. In laboratory experiments on female ruby-throated hummingbirds (Archilochus colubris), probing abilities (maximum extraction depths) increased with increasing corolla diameter. Handling times increased with decreasing corolla diameter, resulting in “handling time equivalents”, i.e., flowers having the same handling times but different lengths and diameters. Longer-billed birds had greater maximum extraction depths and shorter handling times than shorter-billed birds at all corolla diameters greater than the width of the bill. In contrast, shorter-billed birds made fewer errors inserting their bills into narrow flowers. Hence, differences in bill lengths apparently are associated with trade-offs in foraging abilities, whereby longer-billed birds are able to feed at long flowers and may do so more quickly, whereas shorter-billed birds are able to feed more successfully at narrow flowers.

Effect of sexual dimorphism in bill length on foraging behavior: an experimental analysis of hummingbirds

We examined whether sexual differences in trophic morphology are associated with sexual differences in foraging behavior through two laboratory experiments on rufous hummingbirds (Selasphorus rufus) designed to compare probing abilities (maximum extraction depths) and handling times of sexes at flowers. Bills of female S. rufus are about 10.5% longer than bills of males, and this difference was associated with sexual differences in foraging abilities. Maximum extraction depths of female S. rufus were significantly greater than those of males, and no overlap between the sexes was observed. Moreover, handling times of females were shorter than handling times of males at flowers having longer corollas (≥15 mm). Thus, because of their longer bills, female S. rufus have the potential to feed from longer flowers than males, and can do so more quickly. We suggest that no single mechanism is responsible for the evolution of sexual dimorphism in bill lengths of hummingbirds, but rather that the dimorphism probably reflects the combined effects of reproductive role division and intersexual food competition, and possibly, sexual selection.

Evolution of sexual dimorphism in bill size and shape of hermit hummingbirds (Phaethornithinae): a role for ecological causation

Unambiguous examples of ecological causation of sexual dimorphism are rare, and the best evidence involves sexual differences in trophic morphology. We show that moderate female-biased sexual dimorphism in bill curvature is the ancestral condition in hermit hummingbirds (Phaethornithinae), and that it is greatly amplified in species such as Glaucis hirsutus and Phaethornis guy, where bills of females are 60 per cent more curved than bills of males. In contrast, bill curvature dimorphism is lost or reduced in a lineage of short-billed hermit species and in specialist Eutoxeres sicklebill hermits. In the hermits, males tend to be larger than females in the majority of species, although size dimorphism is typically small. Consistent with earlier studies of hummingbird feeding performance, both raw regressions of traits and phylogenetic independent contrasts supported the prediction that dimorphism in bill curvature of hermits is associated with longer bills. Some evidence indicates that differences between sexes of hermit hummingbirds are associated with differences in the use of food plants. We suggest that some hermit hummingbirds provide model organisms for studies of ecological causation of sexual dimorphism because their sexual dimorphism in bill curvature provides a diagnostic clue for the food plants that need to be monitored for studies of sexual differences in resource use.

Mobility of Impatiens capensis flowers: effect on pollen deposition and hummingbird foraging

Flexible pedicels are characteristic of birdpollinated plants, yet have received little attention in studies of hummingbird-flower interactions. A major implication of flexible pedicels is that flowers may move during pollination. We examined whether such motion affected interactions between ruby-throated hummingbirds (Archilochus colubris) and jewelweed (Impatiens capensis) by increasing pollen deposition and by altering the effectiveness of nectar removal. For I. capensis, flower mobility enhanced pollen deposition: birds had significantly longer contact with anthers and more pollen deposited on their bills and crowns when foraging at mobile flowers than at flowers that had been experimentally immobilized. In contrast, flower mobility imposed a cost on hummingbirds by significantly increasing their handling times and reducing their extraction rates relative to their interactions with immobile flowers. Field observations indicated that the motion observed during hummingbird visits did not occur when bees (Bombus spp., Apis mellifera) visited I. capensis flowers, which suggests that the mobility of I. capensis flowers is an adaptation for hummingbird pollination.

Exploitative compensation by subordinate age-sex classes of migrant rufous hummingbirds

SummaryThe three age-sex classes of rufous hummingbirds (Selasphorus rufus) that directly interact on southward migratory stopovers in our California study system differ in territorial ability and resource use. Immature males are behaviorally dominant to adult and immature females and defend the richest territories. Here, we test the hypothesis that the territorially subordinate age-sex classes compensate exploitatively for their exclusion from rich resources. Our results show that females were able to accumulate energy stores at rates comparable to males despite their subordinate territorial status. Territorial females gained body mass at the same rate and in the same pattern as males, and resumed migration at the same body masses. Moreover, during periods when birds were nonterritorial and used dispersed resources, adult and immature females maintained or gained body mass, whereas immature males lost mass. We suggest that females may be energetically compensated by (1) lower costs of flight incurred during foraging and defense, resulting from their lower wing disc loading, and (2) greater success at robbing nectar from rich male territories, resulting from duller coloration (immature females), experience (adult females), and, possibly, hormonal differences. In the future, experiments will be necessary to distinguish the various hypotheses about the mechanisms involved in compensation.

Effect of Nectar Robbery on Phase Duration, Nectar Volume, and Pollination in a Protandrous Plant

We examined the effect of nectar robbery on phase duration of a natural population of Impatiens capensis Meerb. (Balsaminaceae), a species with protandrous flowers. We hypothesized that once robbed, a male‐phase flower should switch its sex from male to female because the probability that the flower would receive enough visits to disperse all its pollen is low compared with the probability that the flower would receive enough visits to fertilize its three to five ovules. We assumed that robbery results in a greater reduction in the attractiveness of male‐phase flowers relative to female‐phase flowers. Field observations supported our hypothesis and its assumptions by demonstrating that natural nectar robbery significantly shortened the duration of male phase. A field experiment in which flowers were experimentally pierced with needles (=flower piercing) showed that the physical damage to the flower caused by piercing alone shortened the duration of male phase. In both the observational and experimental studies, pierced and unpierced flowers did not differ in individual floral life span. Naturally robbed male‐phase flowers contained one‐fifth as much nectar as unrobbed male‐phase flowers, because they either produced less nectar following robbery or had their nectar more frequently removed by robbers. In contrast, naturally robbed and unrobbed female‐phase flowers did not differ significantly in nectar volumes. Naturally robbed male‐phase flowers had 1.4 times as much pollen remaining on their anthers as unrobbed male‐phase flowers, presumably because they were visited less often and for a shorter duration by pollinators. No significant differences in pollen receipt were observed between naturally robbed and unrobbed female‐phase flowers. Our results show that both nectar robbery and flower piercing, and not just rates of pollen removal or seasonal climatic variables, may affect phase duration in dichogamous plants and that any negative effects of nectar robbery and flower piercing on I. capensis plants are likely to occur through male, as opposed to female, function.