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Pie charts indicate proportional likelihoods. Figure 2. Red circles have female song or are migratory, white circles do not. Gray circles are equivocal. The one clade where female song appears to be relatively ancestral is within the genus Myiothlypis.

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The deepest node representing the ancestral warbler has a proportional likelihood of 0. The deepest node has a proportional likelihood of 0. Pruning the tree to remove species with unknown song status due to low research effort results in the same overall reconstruction, with all taxa including Myiothlypis being largely equivocal for female song Table 2.

Overall, the likelihood that ancestral nodes had female song increases when we indicate missing data, but the pattern of evolution of female song is fairly resistant to changes in coding scheme using likelihood methods and under nearly every scheme results indicate many gains of song, but a rate of loss that is at least twice as large as the rate of gain e.

Removing species with missing data does not change the overall pattern, although it does generally improve the likelihood values of the reconstructions Table 2. Migration is recovered as the ancestral state in warblers Figures 2 , 3. Carotenoid dichromatism weak and strong appears to have been gained many times with strong carotenoid dichromatism evolving only twice in Setophaga ruticilla and Setophaga fusca.

Melanin dichromatism, on the other hand, is predominately represented by strong differences between males and females with 34 species exhibiting striking dichromatism and 22 species exhibiting weak dichromatism Figure 4. More dichromatic species were melanin dichromatic than carotenoid dichromatic.

Figure 3. Red circles are dichromatic or migratory, white circles are not. Figure 4. White circles are monochromatic, yellow circles weakly dichromatic, and red circles strongly dichromatic. Most correlation analyses were conducted using song coding scheme 2 female song coded as either present or absent since this coding scheme includes all reports of female song and using other coding schemes doesn't change the resulting correlations. Removing species with low research effort i.

Since removing species with low research effort did not change character correlation results, we used the full tree in all subsequent analyses. As our female song 3 and 4 coding schemes are biologically unrealistic and the character reconstructions were poorly supported we did not run correlation analyses for them.

TiF Checklist: CORE PASSEROIDEA IV — Phaenicophilidae, Icteridae, Parulidae

Table 3. Results of correlation analyses using Pagel's correlation method. The transition rates of the four possible character state combinations in each of three correlations female song 2 vs. Figure 5. Transition rates derived from correlation analyses between A female song 2 and migration, B female song 2 and any plumage dichromatism, and C migration and any plumage dichromatism.

Arrows are scaled to the largest transition rate in each figure. The largest relative rate among two states was switching from being sedentary and having female song to losing female song, with losses occurring 21 times more frequently than gains Figure 5A. Female song was not significantly correlated with migration or plumage dichromatism, so the results of the transition rates between these states should be interpreted with caution. Unexpectedly, given current hypotheses and previously published literature on the distribution of female song in birds Morton, ; Garamszegi et al.

It can be argued that female song is rare, aberrant, or biologically unimportant in species for which we found only one or a few reports of female song.

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This group is generally monochromatic and sedentary and thus conforms to current hypotheses on life history correlates associated with female song. Indeed, all of the duetting species occur in this large clade and duetters account for seven of 12 species reported to sing regularly. However, not all species with frequent female song conform to this pattern, and removing species with rare reports does not change character state reconstructions, only somewhat improves the likelihood of the reconstructions, and does not result in significant correlations between female song and either migration or plumage dichromatism.

Overall the ancestral warbler is reconstructed to not have had singing females. This holds true using different coding schemes for the presence or absence of female song to account for differential research effort. Therefore, we think it much more likely that female song has been repeatedly gained in warblers. Even if we restrict our analysis to species well known to sing or duet, there is not just one origin of this behavior but rather multiple independent origins.

There are only two species branching early in parulid evolution that have reports of female song, the ovenbird Seiurus aurocapilla and the Louisiana waterthrush Parkesia motacilla. Female song in both of these species is thought to be rare, and is likely aberrant in the ovenbird, an extremely well-studied species with only one report of a singing female Hiatt, When rare reports of female song such as these are considered aberrant behavior, then the ancestor of all New World warblers does not reconstruct with female song.

Therefore, we conclude that the ancestral warbler did not have frequent female song and we think it is very likely that it also did not have infrequent female song. Prior studies reconstructing the ancestral state of female song in New World blackbirds Icteridae found song to be equivocal Price, This seemed to be driven by the most basal ingroup Icterid clade, the meadowlarks and allies, which do not have female song.

Given that Parulidae is the sister taxon to Icteridae, it now seems likely that the common ancestor of these groups did not have female song. However, it is also possible that the ancestor of all Icteridae and possibly Parulidae had female song and the loss of female song is derived in the meadowlark clade and also occurred relatively early in warbler evolution. The only characters strongly correlated with each other in our analyses were migration and plumage dimorphism. This is in accordance with other studies of life history correlates of migration in parulids Cardoso and Hu, ; Simpson et al.

There are two major and not necessarily mutually exclusive hypotheses attempting to explain widespread dichromatism in migratory species.

Environmental factors, especially predation, may select for decreased plumage elaboration in migratory females since they are generally not defending territories on the breeding grounds Badyaev and Hill, Alternatively, migratory species have less time to pair and breed, so changes in female plumage may be selected for reduced male aggression toward the female and to facilitate rapid pair-bonding Hamilton, Generally, female dichromatic warblers are less colorful than males, but are usually not cryptically colored and may overall look very similar to males.

Given this pattern, it may be possible that there is selection for reduced male aggression, but not for the cryptic plumage seen in other groups, such as blackbirds, where dichromatism is driven by losses of elaborate carotenoid plumage in females Hofmann et al. In our analyses the ancestral warbler is reconstructed to be a migrant.

This is in agreement with a recent study of the Emberizoidea, which reconstructed the ancestral state of all warblers as north temperate breeders that migrate to the Neotropics Winger et al. Migration is lost in the more recently derived Neotropical clades Myiothlypis, Basileuterus, Cardellina , and Myioborus and only regained twice in the ancestor of the Cardellina group and in M.

Incidentally, this finding is contrary to the long-held hypothesis that migration in birds evolves in the tropics as an escape from competition pressure Levey and Stiles, ; Rappole, ; Rappole and Jones, , particularly given the likely dispersal of the ancestor of the Emberizoidea including warblers into north America from Eurasia over Beringia Barker et al. When counting all 25 parulid species with reports of singing females as indeed having common female song, our analysis found that the evolution of female song is not correlated with losses or gains of migration in this group.

Given that the ancestral warbler was likely migratory and had no female song, it's possible that female song is simply difficult to re-gain even if female song confers higher fitness in sedentary species. In a study comparing the evolution of duetting and migration, an ancestor that is both a duetter and a migrant was found to be five times more likely to lose duetting than to lose migration Logue and Hall, In our study both migrants and non-migrants lose female song at rates 6—20 times higher than they gain it.

Indeed, in all of our correlation analyses with female song, losses of this trait are more common than gains, regardless of migratory status or whether species are dichromatic. These patterns, coupled with the trait reconstructions suggest that female song is often gained independently, but is unstable and easily lost. Such losses are not correlated with migratory status or plumage dichromatism.

Song was lost early in the evolution of warblers possibly before they split from the blackbirds , so female song in warblers likely requires the reactivation of genes and physiological processes involved in song production. Females of many species can be induced to sing with the administration of testosterone Kern and King, ; Nottebohm, ; Langmore, indicating the physiological machinery for song is often in place, but early developmental changes associated with testosterone production may be complicated and difficult to turn back on once lost.

For the purposes of understanding the evolution of female song, a characterization of territoriality in this clade might be informative. Species that are territorial year-round or that maintain a pair bond through the winter are exactly the sort of species we would predict to have female song Benedict, ; Price, While most Neotropical migrants do not seem to be territorial in the winter, some, such as Leiothlypis peregrina Birds of North America , hold winter territories, and are thus territorial year-round. Unfortunately, few data exist on these traits for most species of warblers, precluding more detailed analysis.

The ancestral warbler is reconstructed as being monochromatic in both separate analyses of carotenoid and melanin dichromatism, and is equivocal when reconstructing any dichromatism. We think it more likely that the ancestor was monochromatic given that extant species near the base of the warbler tree are dichromatic. Existing studies have shown that either monochromatism Malacarne et al. Our reconstruction indicates that parulid warblers underwent an early shift to dichromatism, but that gains of female song were not correlated with either losses or gains of melanin, carotenoid, or general dichromatism Table 3.

Female song appears much more labile than plumage characteristics as both transitions toward and away from female song were much larger than changes in plumage state Figure 5B. Combined with other research, our study adds to the argument that there is no clear pattern of association between the presence of female song and dichromatism, suggesting that these traits may evolve relatively independently Mason et al.

A recent study of the evolution of dichromatism in parulid warblers concluded that the common ancestor was monochromatic and bright Simpson et al. Overall, our data suggest that dichromatism in this group is driven more by changes in melanin pigmentation than carotenoid pigmentation often yellow in females. Only two species were strongly dimorphic in carotenoid pigmentation, while 34 species were strongly dimorphic in melanin pigmentation. Whether the ancestor of warblers was ornamented or not is equivocal and should be the subject of future study. In contrast with this pattern in parulids, plumage dichromatism in orioles genus Icterus is driven specifically by losses of bright plumage both melanins and carotenoids in females Hofmann et al.

Regardless, monochromatic blackbird species tend to have female song and we found a similar although statistically unsupported trend in warbler species with common female song.

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Among Parulid warblers, female song is not correlated with migratory status, melanin or carotenoid dichromatism, even though migration and plumage dichromatism are correlated with each other. Nearly all species that duet are sedentary and monochromatic, but the presence of dichromatic and migratory species with female song prevent any correlation of losses of song with losses of migration.

This result counters our predictions based on similar studies and suggests that gains of female song may evolve due to different selective pressures than losses of female song. In contrast, the correlated evolution of migration and plumage dichromatism may indicate that coloration in this group evolves following many of the same pressures that other species notably the Icterid blackbirds face when adopting a migratory or sedentary strategy. Additionally, the different prevalence of female song in these two families may simply reflect the fact that blackbirds gained female song early in their radiation and warblers did not.

If gains and losses of female song occur at different rates, then ancestral condition can set clades on very distinct evolutionary trajectories.

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NN and LB wrote the paper and scored plumage characters. NN scored song and migration characters and ran analyses in Mesquite. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. We'd like to thank Irby Lovette for providing us with the warbler phylogeny. Mitchell McGlaughlin for help and advice about using Mesquite, and Nora Covy for scoring plumage characters. Armenta, J. Quantifying avian sexual dichromatism: a comparison of methods.