The tangled evolutionary history of a long-debated Mesoamerican taxon: The Velazquez Woodpecker (Melanerpes santacruzi, Aves: Picidae).

The Velazquez Woodpecker Melanerpes santacruzi is a highly polytypic species distributed from east-central Mexico to northern Nicaragua. The ample variation in body size, barring of the plumage, and the coloration of nasal tufts, neck, and belly have fueled debates about the taxonomy and evolutionary history of the species; however, the processes generating these patterns of variation and the underlying population dynamics throughout the species' distribution remain poorly understood. Here, we employed reduced representation genome sequencing (NextRAD) and Ecological Niche Modeling methods to test the distinctiveness of the Velazquez Woodpecker based on this new set of genomic data and analyze the correspondence of the genetic structure and ecological differentiation with phenotypic variation and geographic distribution. From phylogenetic and demographic analyses including the Golden-Fronted (M. aurifrons) and Red-bellied Woodpecker (M. carolinus), we obtained results congruent with previous molecular phylogenies. The clades of M. santacruzi and M. carolinus-M. aurifrons are reciprocally monophyletic, although the sister group relationship of M. aurifrons is ambiguous. Using genetic and ecological analyses, we found that the species is structured into three genetically and ecologically differentiated groups comprising the subspecies (1) M. s. santacruzi, (2) M. s. dubius and (3) M. s. grateloupensis-polygrammus-veraecrucis. These groups diverged recently, with two splits between 250,000 and 150,000 years ago, and show a significant genetic admixture among them, especially in their current contact zones. Ecological and demographic models suggest the existence of intermittent areas of sympatry and connectivity among populations of M. santacruzi since the Last Interglacial period. We also found evidence of bi-directional gene flow between the species M. aurifrons and the nearby populations of M. santacruzi (M. s. grateloupensis), along the Sierra Madre Oriental in northeastern Mexico. Gene flow seems to be uneven, with prevalence of movement in the direction from M. aurifrons to M. s. grateloupensis.

Description and molecular characterization of novel Leucocytozoon parasite (Apicomplexa: Haemosporida: Leucocytozoidae), Leucocytozoon polynuclearis n. sp. found in North American woodpeckers.

We describe Leucocytozoon polynuclearis n. sp. (Haemosporida: Leucocytozoidae) from two North American woodpeckers, the northern flicker (Colaptes auratus Linnaeus) and white-headed woodpecker (Dryobates albolarvatus Boie, 1826), based on the morphology of its blood stages and portions of the mitochondrial cytochrome b gene. The most distinctive features of Leucocytozoon polynuclearis n. sp. development are the triangular-shaped host cell nuclei and position of host cell nuclei above gametocytes. This parasite inhabits thrombocytes. Leucocytozoon squamatus Nandi, 1986, the only other Leucocytozoon species detected from Picidae birds, lacks features that are commonly found with L. polynuclearis n. sp. infections. Phylogenetic analysis identified DNA lineages associated with L. polynuclearis n. sp. and showed that this parasite is more closely related to other North American Leucocytozoon species than to L. squamatus, whose initial description was from infected Old World Picidae species. Although there are reports of L. squamatus in North American Picidae species, these detections were based only on microscopic examinations, remain genetically non-characterized, and might be misidentifications with regards to L. polynuclearis n. sp. Available parasite distribution data indicate that L. polynuclearis n. sp. infects Picidae species throughout North America and L. squamatus distribution probably is restricted to Old World Piciformes birds.

The correct genus for the Afrotropical woodpeckers Campethera caroli and Campethera nivosa (Aves: Piciformes, Picidae).

We argue that the correct generic name for the Afrotropical woodpeckers usually known as Campethera caroli and Campethera nivosa (Aves: Piciformes, Picidae) should be Pardipicus Bonaparte, 1854, and we choose and propose Chloropicus caroli Malherbe, 1852 as type species. Fuchs et al. (2018) had suggested Stictopicus Malherbe, 1861, following Wolters (1977), but that genus has as type species Picus nubicus Boddaert, 1783 (= Campethera nubica).

Global relationships between tree-cavity excavators and forest bird richness.

Global monitoring of biodiversity and ecosystem change can be aided by the effective use of indicators. Tree-cavity excavators, the majority of which are woodpeckers (Picidae), are known to be useful indicators of the health or naturalness of forest ecosystems and the diversity of forest birds. They are indicators of the latter due to shared associations with particular forest elements and because of their role in facilitating the occurrence of other species through the provision of nesting cavities. Here, we investigated whether these positive correlations between excavators and other forest birds are also found at broad geographical scales. We used global distribution maps to extract richness estimates of tree-cavity nesting and forest-associated birds, which we grouped by zoogeographic regions. We then created generalized least-squares models to assess the relationships between these groups of birds. We show that richness of tree-cavity excavating birds correlates positively with that of secondary cavity nesters and other forest birds (generalists and specialists) at global scales, but with variation across zoogeographic regions. As many excavators are relatively easy to detect, play keystone roles at local scales and are effective management targets, we propose that excavators are useful for biodiversity monitoring across multiple spatial scales and geographical regions, especially in the tropics.

A review of the feather mite family Gabuciniidae Gaud amp; Atyeo (Acariformes: Astigmata: Pterolichoidea) of Brazil, with descriptions of eleven new species.

The feather mite family Gabuciniidae currently includes 16 genera and approximately 65 described species associated with birds of nine orders, with the greatest diversity on Accipitriformes. In this study, 11 new species are described from the following hosts: Aetacarus accipiter sp. nov. from the Bicolored Hawk Accipiter bicolor (Vieillot, 1817) (Accipitriformes: Accipitridae), Capitolichus campoflicker sp. nov. from the Campo Flicker Colaptes campestris (Vieillot, 1818) (Piciformes: Picidae), Coraciacarus cabure sp. nov. from the Barred Forest-falcon Micrastur ruficollis (Vieillot, 1817) (Falconiformes: Falconidae), Coraciacarus peixefrito sp. nov. from the Pheasant Cuckoo Dromococcyx phasianellus (Spix, 1824) (Cuculiformes: Cuculidae), Gabucinia neotropica sp. nov. from the Curl-crested Jay Cyanocorax cristatellus (Temminck, 1823) (type host) and C. chrysops (Vieillot, 1818) (Passeriformes: Corvidae), Hieracolichus caboclo sp. nov. from the Savanna Hawk Buteogallus meridionalis (Latham, 1790) (Accipitriformes: Accipitridae), Hieracolichus falcon sp. nov. from the Southern Caracara Caracara plancus (Miller, 1777) (Falconiformes: Falconidae), Piciformobia adjuncta sp. nov. from the Guira Cuckoo Guira guira (Gmelin, 1788) (Cuculiformes: Cuculidae), Proaposolenidia bicolor sp. nov. from the Bicolored Hawk Accipiter bicolor (Vieillot, 1817) (Accipitriformes: Accipitridae), Proaposolenidia plumbea sp. nov. from the Plumbeous Kite Ictinia plumbea (Gmelin, 1788) (Accipitriformes: Accipitridae), and Tocolichus toco sp. nov. from the Toco Toucan Ramphastos toco Statius Müller, 1776 (Piciformes: Ramphastidae). In addition, two new combinations are proposed, Proaposolenidia ostoda (Gaud, 1983) comb. nov. and Aetacarus hirundo (Mégnin Trouessart, 1884) comb. nov., both transferred from the genus Hieracolichus. With the addition of these new species, the number of gabuciniids described from the Neotropical region has increased from 14 to 25 species. These findings indicate that Brazil is home to a large diversity of undescribed gabuciniids, which is not surprising considering the vast bird fauna of this country, and especially since most avian species from Brazil have yet to be investigated for their feather mites.

Haemoproteosis lethality in a woodpecker, with molecular and morphological characterization of Haemoproteus velans (Haemosporida, Haemoproteidae).

A juvenile White-headed woodpecker (Dryobates albolarvatus) fitted with a radio tag was located dead at approximately 22-days post-fledging in Yakima county in central Washington in July 2015. Postmortem examination revealed an enlarged liver and spleen plus evidence of iron sequestration. Microscopic examination observed young gametocytes within the cytoplasm of erythrocytes, and exo-erythrocytic meronts within the cytoplasm of capillary endothelial cells, hepatocytes, and myocytes, and free in the tissues. These attributes implicated a haemosporidian infection that likely resulted in mortality. Subsequent sampling results of local woodpecker species in the same area during the breeding season in June-July 2016 and May-July 2017 showed other individuals infected with Haemoproteus parasites. Nested Polymerase Chain Reaction (PCR), sequencing, and microscopic analyses for avian haemosporidians revealed infections with Haemoproteus velans (Haemosporida, Haemoproteidae). This parasite was characterized molecularly and morphologically. This is the first report of a haemosporidian infection in a White-headed woodpecker anywhere in its range, and the first reported suspected mortality from haemoproteosis for a woodpecker (Piciformes, Picidae). The use of radio-tagged birds is an asset in wildlife haemosporidian studies because the effect of the pathogen can be monitored in real time. Additionally, this methodology provides opportunities to collect fresh material for microscopic and histological examination from wild birds that have died from natural causes.

Two new mitogenomes of Picidae (Aves, Piciformes): Sequence, structure and phylogenetic analyses.

The family Picidae is classified in the order Piciformes with 236 recognized species in 35 genera. Phylogenetic relationships within the Piciformes are still unresolved by major cause of plumage convergence. This study presented two new mitogenomes of Picidae, Darjeeling woodpecker (Dendrocopos darjellensis) and Gray-capped woodpecker (Yungipicus canicapillus), with the size of 16,727 and 16,847 bp, respectively. They have the identical gene order: 37 genes, including 13 PCGs, two rRNA genes, 22 tRNA genes, and two control regions. Furthermore, an extra cytosine insertion at position 174 of MT-ND3 was also found in both species. The MT-RNR1 of Y. canicapillus shared 89.0% nucleotide sequence identity and a similar secondary structure with that of D. darjellensis, consisting of 46 helices and three main domains. There is more divergence in the MT-RNR2 secondary structures than those of MT-RNR1 between the two species. We found the highest dN/dS for the MT-ATP8 (0.08326) among Piciformes, while the lowest for the MT-CO1 (0.00802). Our phylogenetic analyses suggested that the subfamily Picumninae is paraphyletic, and D. darjellensis had a closer relationship with D. major than D. leucotos. The findings of the present study will be useful for further investigating the evolutionary relationships within Piciformes.

Tapping the woodpecker tree for evolutionary insight.

Molecular phylogenetic studies of woodpeckers (Picidae) have generally focused on relationships within specific clades or have sampled sparsely across the family. We compared DNA sequences of six loci from 203 of the 217 recognized species of woodpeckers to construct a comprehensive tree of intrafamilial relationships. We recovered many known, but also numerous unknown, relationships among clades and species. We found, for example, that the three picine tribes are related as follows (Picini, (Campephilini, Melanerpini)) and that the genus Dinopium is paraphyletic. We used the tree to analyze rates of diversification and biogeographic patterns within the family. Diversification rate increased on two occasions during woodpecker history. We also tested diversification rates between temperate and tropical species but found no significant difference. Biogeographic analysis supported an Old World origin of the family and identified at least six independent cases of New World-Old World sister relationships. In light of the tree, we discuss how convergence, mimicry, and potential cases of hybridization have complicated woodpecker taxonomy.

Complex biogeographic scenarios revealed in the diversification of the largest woodpecker radiation in the New World.

Phylogenetic relationships and patterns of evolution within Melanerpes, one of the most diverse groups of New World woodpeckers (22-23 lineages), have been complicated due to complex plumages and morphological adaptations. In an attempt to resolve these issues, we obtained sequence data from four nuclear introns and two mitochondrial protein-coding genes for 22 of the 24 currently recognized species in the genus. We performed phylogenetic analyses involving Maximum Likelihood and Bayesian Inference, species-tree divergence dating, and biogeographic reconstructions. Tree topologies from the concatenated and species-tree analyses of the mtDNA and nDNA showed broadly similar patterns, with three relatively well-supported groups apparent: (a) the Sphyrapicus clade (four species); (b) the typical Melanerpes clade, which includes temperate and subtropical dry forest black-backed species; and (c) the mostly barred-backed species, here referred to as the "Centurus" clade. The phylogenetic position of Melanerpes superciliaris regarding the rest of Melanerpes is ambiguous as it is recovered as sister to the rest of Melanerpes or as sister to a group including Sphyrapicus+Melanerpes. Our species tree estimations recovered the same well-delimited highly-supported clades. Geographic range evolution (estimated in BioGeoBEARS) was best explained by a DIVALIKE+j model, which includes vicariance, founder effect speciation, and anagenetic dispersal (range expansion) as important processes involved in the diversification of the largest radiation of woodpeckers in the New World.

Biogeography and diversification dynamics of the African woodpeckers.

The dynamics of species accumulation of African terrestrial vertebrates over time remains underexplored in comparison with those in the New World, despite Africa hosting about 25% of the world's avian diversity. This lack of knowledge hampers our understanding of the fundamental processes that drive biodiversity and the dynamics of speciation. To begin to address this gap, we reconstructed species-level phylogenies of two unrelated clades of African woodpeckers (12 species of Geocolaptes/Campethera and 13 species of Chloropicus/Mesopicos/Dendropicos/Ipophilus) that diverged from their closest Indo-Malayan relatives at similar times. Our results demonstrate that the current taxonomy is misleading: three (Campethera, Dendropicos and Mesopicos) out of four polytpic genera/subgenera are not monophyletic. Our results also show that current estimates of diversity at the species level are significantly understated, as up to 18 species for the 'Campethera clade' and 19 for the 'Dendropicos clade' could be recognized. The first splits within both clades involve species that are largely restricted to the Guineo-Congolian biogeographic regions, followed by later adaptations to particular habitats (forest versus savannah) and colonization of other regions (e.g. Southern Africa), each of which occurred multiple times in both clades. Assuming a conservative species delimitation scheme, our results indicate that diversification rates are decreasing through time for both clades. Applying a more extreme species recognition scheme (18 and 19 species for the Campethera and Dendropicos clades, respectively), our results support a decrease in diversification rates only for the Dendropicos clade and thus underline the importance of the number of species included in our diversification analyses. Greater ecological diversity of the Campethera clade where multiple species exhibit either an arboreal or terrestrial foraging strategy might explain the constant diversification rates through time we found under the eighteen species scheme.

An augmented supermatrix phylogeny of the avian family Picidae reveals uncertainty deep in the family tree.

The accumulation of DNA sequence data in public repositories allows for phylogenetic inference on unprecedented taxonomic scales using supermatrix approaches. Careful analysis of available data allows strategic augmentation with new sequences in order to maximize taxonomic sampling and coverage of informative loci. I inferred relationships among 179 species (76%) in the avian family Picidae (woodpeckers, piculets, and wrynecks), using publicly available sequence data supplemented with targeted sequencing to increase species-level and locus-level sampling and maximize resolution. Results of these analyses generally corroborate previous molecular studies, with consensus on the membership of most genera and tribes. However, several newly placed taxa show surprising affinities, and several genera as currently delineated appear to be paraphyletic. Relationships among major clades of Picidae remain poorly resolved, particularly among the three lineages of piculets, the unusual woodpecker genus Hemicircus, and the remaining woodpeckers, and among the major groups of true woodpeckers (Picinae). If these deep relationships are to be resolved, phylogenomic approaches may be necessary.

Fruit consumption by four woodpecker species (PICIDAE: AVES) in semideciduous seasonal forest remnants of South Brazil

Este estudio se realizó entre 1990 y 1997, en dos fragmentos del bosque estacional semidecidual en el Estado de Paraná, Brasil, y examinó el consumo de frutas por cuatro especies de carpinteros (Melanerpes flavifrons, Veniliornis spilogaster, Colaptes melanochloros y Celeus flavescens). La dieta de estas especies fue evaluada a través de dos métodos complementarios: registros visuales y análisis de muestras fecales. Se obtuvieron 41 registros visuales y 23 muestras fecales, de que más de la mitad contenían semillas de un o más especies, en cantidades variables (1 a 100). En todo, fueron identificadas trece especies de frutas, cuyas características se presentan y discuten. Al contrario de lo esperado, el consumo de frutas fue más grande durante el periodo de menos disponibilidad de este recurso en las áreas estudiadas, es decir, entre octubre y marzo. Desde que éste es el periodo en que la mayoría de estas aves se reproducen, y también la cumbre de disponibilidad de insectos, se discute el consumo de frutas cuanto a balanceo nutritivo y enérgico, sobre todo para las aves jóvenes que se mantienen en el nido. Datos sobre la captura de estas especies son presentados en detalle, con el objetivo de estimular otros estudios que pueden contribuir para el mejor entendimiento de la biología de los Picidae neotropicales.